Mutual inactivation of Notch receptors and ligands facilitates developmental patterning

PLoS Computational Biology

Volumn 7, Issue 6, 2011, Pages

  Sprinzak, David ^a,b   Lakhanpal, Amit ^a,b   LeBon, Lauren ^a,b   Garcia Ojalvo, Jordi ^c   Elowitz, Michael B ^a,b  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b California Institute of Technology   (United States)

^c UNIVERSITAT POLITÈCNICA DE CATALUNYA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SIGNALING; LIGANDS;

DROSOPHILLA; FORMATION PROCESS; INDIVIDUAL CELLS; JUXTACRINE SIGNALING; LATERAL INHIBITION; NOTCH RECEPTOR; PATTERN FORMATION; SIGNALING LIGANDS; SIGNALING RECEPTOR; SWITCHING BEHAVIORS;

GENE EXPRESSION;

DROSOPHILA PROTEIN; INSECT PROTEIN; JAGGED1; LIGAND; MORPHOGEN; NOTCH RECEPTOR; PROTEIN LAG2; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; PROTEIN; SIGNAL PEPTIDE;

ANALYTIC METHOD; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DELTA GENE; DEVELOPMENTAL GENE; DROSOPHILA; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INACTIVATION; GENE INTERACTION; GENETIC CODE; INTRACELLULAR SIGNALING; LAG2 GENE; MATHEMATICAL MODEL; NOTCH RECEPTOR GENE; SERRATE GENE; VASCULARIZATION; ALGORITHM; ANIMAL; CELL COMMUNICATION; CHEMICAL STRUCTURE; METABOLISM; MORPHOGENESIS; PHYSIOLOGY;

METAZOA;

ALGORITHMS; ANIMALS; BODY PATTERNING; CELL COMMUNICATION; DROSOPHILA; DROSOPHILA PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MODELS, MOLECULAR; RECEPTORS, NOTCH;

EID: 79959843692     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002069     Document Type: Article

References (42)

1. Huppert SS, Jacobsen TL, Muskavitch MA, (1997) Feedback regulation is central to Delta-Notch signalling required for Drosophila wing vein morphogenesis. Development 124: 3283-3291.
2. de Celis JF, Bray S, Garcia-Bellido A, (1997) Notch signalling regulates veinlet expression and establishes boundaries between veins and interveins in the Drosophila wing. Development 124: 1919-1928.
3. Heitzler P, Simpson P, (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64: 1083-1092.
4. Bray SJ, (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7: 678-689.
5. de Celis JF, Bray S, (1997) Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development 124: 3241-3251.
6. Micchelli CA, Rulifson EJ, Blair SS, (1997) The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate. Development 124: 1485-1495.
7. Klein T, Brennan K, Arias AM, (1997) An intrinsic dominant negative activity of serrate that is modulated during wing development in Drosophila. Dev Biol 189: 123-134.
8. Li Y, Baker NE, (2004) The roles of cis-inactivation by Notch ligands and of neuralized during eye and bristle patterning in Drosophila. BMC Dev Biol 4: 5.
9. Matsuda M, Chitnis AB, (2009) Interaction with Notch determines endocytosis of specific Delta ligands in zebrafish neural tissue. Development 136: 197-206.
10. Miller AC, Lyons EL, Herman TG, (2009) cis-Inhibition of Notch by endogenous Delta biases the outcome of lateral inhibition. Curr Biol 19: 1378-1383.
11. Sprinzak D, Lakhanpal A, Lebon L, Santat LA, Fontes ME, et al. (2010) Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 465: 86-90.
12. Becam I, Fiuza UM, Arias AM, Milan M, (2010) A role of receptor notch in ligand cis-inhibition in Drosophila. Curr Biol 20: 554-560.
13. Sakamoto K, Ohara O, Takagi M, Takeda S, Katsube K, (2002) Intracellular cell-autonomous association of Notch and its ligands: a novel mechanism of Notch signal modification. Dev Biol 241: 313-326.
14. Glittenberg M, Pitsouli C, Garvey C, Delidakis C, Bray S, (2006) Role of conserved intracellular motifs in Serrate signalling, cis-inhibition and endocytosis. EMBO J 25: 4697-4706.
15. Meinhardt H, (1982) Models of biological pattern formation. London; New York Academic Press. xi, 230 p. p.
16. Plahte E, (2001) Pattern formation in discrete cell lattices. J Math Biol 43: 411-445.
17. Meinhardt H, Gierer A, (1980) Generation and regeneration of sequence of structures during morphogenesis. J Theor Biol 85: 429-450.
18. Sturtevant MA, Roark M, Bier E, (1993) The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the EGF-R signaling pathway. Genes Dev 7: 961-973.
19. de Celis JF, Bray SJ, (2000) The Abruptex domain of Notch regulates negative interactions between Notch, its ligands and Fringe. Development 127: 1291-1302.
20. Vassin H, Vielmetter J, Campos-Ortega JA, (1985) Genetic interactions in early neurogenesis of Drosophila melanogaster. J Neurogenet 2: 291-308.
21. Barad O, Rosin D, Hornstein E, Barkai N, (2010) Error minimization in lateral inhibition circuits. Sci Signal 3: ra51.
22. Losick R, Desplan C, (2008) Stochasticity and cell fate. Science 320: 65-68.
23. Elowitz MB, Levine AJ, Siggia ED, Swain PS, (2002) Stochastic gene expression in a single cell. Science 297: 1183-1186.
24. Goodyear R, Richardson G, (1997) Pattern formation in the basilar papilla: evidence for cell rearrangement. J Neurosci 17: 6289-6301.
25. Collier JR, Monk NA, Maini PK, Lewis JH, (1996) Pattern formation by lateral inhibition with feedback: a mathematical model of delta-notch intercellular signalling. J Theor Biol 183: 429-446.
26. Othmer HG, Scriven LE, (1971) Instability and dynamic pattern in cellular networks. J Theor Biol 32: 507-537.
27. Wilkinson HA, Fitzgerald K, Greenwald I, (1994) Reciprocal changes in expression of the receptor lin-12 and its ligand lag-2 prior to commitment in a C. elegans cell fate decision. Cell 79: 1187-1198.
28. Ferrell JE, Xiong W, (2001) Bistability in cell signaling: How to make continuous processes discontinuous, and reversible processes irreversible. Chaos 11: 227-236.
29. Saiz L, Vilar JM, (2006) DNA looping: the consequences and its control. Curr Opin Struct Biol 16: 344-350.
30. Kuhlman T, Zhang Z, Saier MH Jr, Hwa T, (2007) Combinatorial transcriptional control of the lactose operon of Escherichia coli. Proc Natl Acad Sci U S A 104: 6043-6048.
31. Dueber JE, Mirsky EA, Lim WA, (2007) Engineering synthetic signaling proteins with ultrasensitive input/output control. Nat Biotechnol 25: 660-662.
32. Buchler NE, Louis M, (2008) Molecular titration and ultrasensitivity in regulatory networks. J Mol Biol 384: 1106-1119.
33. Levine E, Zhang Z, Kuhlman T, Hwa T, (2007) Quantitative characteristics of gene regulation by small RNA. PLoS Biol 5: e229.
34. Elf J, Paulsson J, Berg OG, Ehrenberg M, (2003) Near-critical phenomena in intracellular metabolite pools. Biophys J 84: 154-170.
35. Mehta P, Goyal S, Wingreen NS, (2008) A quantitative comparison of sRNA-based and protein-based gene regulation. Mol Syst Biol 4: 221.
36. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, et al. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118: 69-82.
37. Buchler NE, Cross FR, (2009) Protein sequestration generates a flexible ultrasensitive response in a genetic network. Mol Syst Biol 5: 272.
38. Levine E, Hwa T, (2008) Small RNAs establish gene expression thresholds. Curr Opin Microbiol 11: 574-579.
39. Heitzler P, (1993) Altered epidermal growth factor-like sequences provide evidence for a role of Notch as a receptor in cell fate decisions. Development 117: 1113-1123.
40. Fryer CJ, White JB, Jones KA, (2004) Mastermind recruits CycC:CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover. Mol Cell 16: 509-520.
41. Seugnet L, Simpson P, Haenlin M, (1997) Transcriptional regulation of Notch and Delta: requirement for neuroblast segregation in Drosophila. Development 124: 2015-2025.
42. Parks AL, Shalaby NA, Muskavitch MA, (2008) Notch and suppressor of Hairless regulate levels but not patterns of Delta expression in Drosophila. Genesis 46: 265-275.