Multiple feedback loops achieve robust localization of wingless expression in Drosophila notum development

Journal of Theoretical Biology

Volumn 292, Issue , 2012, Pages 18-29

  Hironaka, Ken ichi ^a   Iwasa, Yoh ^a   Morishita, Yoshihiro ^a,b  

^a KYUSHU UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Gene regulatory network; Morphogen; Network motif; Positional information; Systems biology

Indexed keywords

MORPHOGEN; WNT1 PROTEIN;

BIOLOGICAL ANALYSIS; GENE EXPRESSION; MORPHOGENESIS; NUMERICAL MODEL;

ARTICLE; DROSOPHILA; ENZYME ACTIVATION; ENZYME REGULATION; FEEDBACK SYSTEM; GENE; INSECT DEVELOPMENT; INSECT GENETICS; MOLECULAR DYNAMICS; MORPHOGENESIS; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; WG GENE;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENES, INSECT; MORPHOGENESIS; NUCLEOTIDE MOTIFS; WNT1 PROTEIN;

DROSOPHILA NOTUM;

EID: 80053487753     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2011.09.022     Document Type: Article

References (60)

1. Alon U. An introduction to systems biology: design principles of biological circuits 2007, CRC Press.
2. Alon U. Network motifs: theory and experimental approaches. Nat. Rev. Genet. 2007, 8:450-461.
3. Andrianantoandro E., Basu S., Karig D.K., Weiss R. Synthetic biology: new engineering rules for an emerging discipline. Mol. Syst. Biol. 2006, 2.
4. Basu S., Mehreja R., Thiberge S., Chen M.-T., Weiss R. Spatiotemporal control of gene expression with pulse-generating networks. Proc. Natl. Acad. Sci. U. S. A 2004, 101:6355-6360.
5. Benner S.A., Sismour A.M. Synthetic biology. Nat. Rev. Genet. 2005, 6:533-543.
6. Blake W.J., Kaern M., Cantor C.R., Collins J.J. Noise in eukaryotic gene expression. Nature 2003, 422:633-637.
7. Brook W.J., Diaz-Benjumea F.J., Cohen S.M. Organizing spatial pattern in limb development. Annu. Rev. Cell Dev. Biol. 1996, 12:161-180.
8. Calleja M., Herranz H., Estella C., Casal J., Lawrence P., Simpson P., Morata G. Generation of medial and lateral dorsal body domains by the pannier gene of Drosophila. Development 2000, 127:3971-3980.
9. Cardoso W., Lü J. Regulation of early lung morphogenesis: questions, facts and controversies. Development 2006, 133:1611-1624.
10. de Celis J., Barrio R., Kafatos F. Regulation of the spalt/spalt-related gene complex and its function during sensory organ development in the Drosophila thorax. Development 1999, 126:2653-2662.
11. Eldar A., Rosin D., Shilo B.-Z., Barkai N. Self-enhanced ligand degradation underlies robustness of morphogen gradients. Dev. Cell 2003, 5:635-646.
12. Elowitz M.B., Levine A.J., Siggia E.D., Swain P.S. Stochastic gene expression in a single cell. Science 2002, 297:1183-1186.
13. Entchev E., Schwabedissen A., Gonz lez-Gait n M. Gradient formation of the TGF-Β homolog Dpp. Cell 2000, 103:981-991.
14. Ferrell J., Xiong W. Bistability in cell signaling: how to make continuous processes discontinuous, and reversible processes irreversible. Chaos 2001, 11:227-236.
15. Funakoshi Y., Minami M., Tabata T. mtv shapes the activity gradient of the Dpp morphogen through regulation of thick veins. Development 2001, 128:67-74.
16. Garcia-Garcia M.J., Ramain P., Simpson P., Modolell J. Different contributions of pannier and wingless to the patterning of the dorsal mesothorax of Drosophila. Development 1999, 126:3523-3532.
17. Ghazi A. Prepattern genes and signaling molecules regulate stripe expression to specify Drosophila flight muscle attachment sites. Mech. Dev 2003, 120:519-528.
18. Gilbert S. Development biology 1988, Sinauer Associates.
19. Goldbeter A., Koshland D. An amplified sensitivity arising from covalent modification in biological systems. Proc. Natl. Acad. Sci. U. S. A 1981, 78:6840-6844.
20. Gregor T., Tank D.W., Wieschaus E.F., Bialek W. Probing the limits to positional information. Cell 2007, 130:153-164.
21. 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.
22. Hasty J., McMillen D., Isaacs F., Collins J.J. Computational studies of gene regulatory networks: in numero molecular biology. Nat. Rev. Genet. 2001, 2:268-279.
23. Hirashima T., Iwasa Y., Morishita Y. Distance between AER and ZPA Is defined by feed-forward loop and is stabilized by their feedback loop in vertebrate limb bud. Bull. Math. Biol. 2008, 70:438-459.
24. Houchmandzadeh B., Wieschaus E., Leibler S. Establishment of developmental precision and proportions in the early Drosophila embryo. Nature 2002, 415:798-802.
25. Houchmandzadeh B., Wieschaus E., Leibler S. Precise domain specification in the developing Drosophila embryo. Phys. Rev. E 2005, 72:061920.
26. Inoue H., Imamura T., Ishidou Y., Takase M., Udagawa Y., Oka Y., Tsuneizumi K., Tabata T., Miyazono K., Kawabata M. Interplay of signal mediators of decapentaplegic (Dpp): molecular characterization of mothers against dpp, Medea, and daughters against dpp. Mol. Biol. Cell 1998, 9:2145-2156.
27. Ishihara S., Fujimoto K., Shibata T. Cross talking of network motifs in gene regulation that generates temporal pulses and spatial stripes. Genes Cells 2005, 10:1025-1038.
28. Kaplan S., Bren A., Dekel E., Alon U. The incoherent feed-forward loop can generate non-monotonic input functions for genes. Mol. Syst. Biol. 2008, 4:203.
29. Kerszberg M., Wolpert L. Mechanisms for positional signalling by morphogen transport: a theoretical study. J. Theor. Biol. 1998, 191:103-114.
30. Kim D., Kwon Y.-K., Cho K.-H. The biphasic behavior of incoherent feed-forward loops in biomolecular regulatory networks. Bioessays 2008, 30:1204-1211.
31. Koshland D.E. Switches, thresholds and ultrasensitivity. Trends Biochem. Sci. 1987, 12:225-229.
32. Lander A., Nie Q., Wan F. Do morphogen gradients arise by diffusion?. Dev. Cell 2002, 2:785-796.
33. Latinkic B.V., Umbhauer M., Neal K.A., Lerchner W., Smith J.C., Cunliffe V. The Xenopus Brachyury promoter is activated by FGF and low concentrations ofactivinandsuppressed by high concentrationsof activin and by paired-type homeodomain proteins. Genes Dev. 1997, 11:3265-3276.
34. Laufer E., Nelson C.E., Johnson R.L., Morgan B.A., Tabin C. Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 1994, 79:993-1003.
35. Laurent M., Kellershohn N. Multistability: a major means of differentiation and evolution in biological systems. Trends Biochem. Sci. 1999, 24:418-422.
36. Letizia A., Barrio R., Campuzano S. Antagonistic and cooperative actions of the EGFR and Dpp pathways on the iroquois genes regulate Drosophila mesothorax specification and patterning. Development 2007, 134:1337-1346.
37. Mangan S., Alon U. Structure and function of the feed-forward loop network motif. Proc. Natl. Acad. Sci. U. S. A 2003, 100:11980-11985.
38. Mangan S., Itzkovitz S., Zaslaver A., Alon U. The Incoherent Feed-forward Loop Accelerates the Response-time of the gal System of Escherichia coli. J. Mol. Biol. 2006, 356:1073-1081.
39. Massagué J. TGF-Β SIGNAL TRANSDUCTION. Annu. Rev. Biochem. 1998, 67:753-791.
40. McDowell N., Gurdon J., Grainger D. Formation of a functional morphogen gradient by a passive process in tissue from the early Xenopus embryo. Int. J. Dev. Biol. 2001, 45:199-208.
41. Milo R., Shen-Orr S., Itzkovitz S., Kashtan N., Chklovskii D., Alon U. Network Motifs: Simple Building Blocks of Complex Networks. Science 2002, 298:824-827.
42. Modolell J., Campuzano S. The achaete-scute complex as an integrating device. Int. J. Dev. Biol. 1998, 42:275-282.
43. Morishita Y., Iwasa Y. Optimal placement of multiple morphogen sources. Phys. Rev. E 2008, 77:041909.
44. Morishita Y., Iwasa Y. Accuracy of positional information provided by multiple morphogen gradients with correlated noise. Phys. Rev. E 2009, 79:061905.
45. Niswander L., Jeffrey S., Martin G., Tickle C. A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 1994, 371:609-612.
46. Ogiso Y., Tsuneizumi K., Masuda N., Sato M., Tabata T. Robustness of the Dpp morphogen activity gradient depends on negative feedback regulation by the inhibitory Smad,. Dad. Dev. Growth Differ. 2011, 53:668-678.
47. Pfeiffer S., Vincent J. Signalling at a distance: transport of wingless in the embryonic epidermis of Drosophila. Semin. Cell Dev. Biol. 1999, 10:303-309.
48. Sato M., Saigo K. Involvement of pannier and u-shaped in regulation of Decapentaplegic-dependent wingless expression in developing Drosophila notum. Mech. Dev. 2000, 93:127-138.
49. Sato M., Kojima T., Michiue T., Saigo K. Bar homeobox genes are latitudinal prepattern genes in the developing Drosophila notum whose expression is regulated by the concerted functions of decapentaplegic and wingless. Development 1999, 126:1457-1466.
50. Savageau M. Parameter Sensitivity as a Criterion for Evaluating and Comparing the Performance of Biochemical Systems. Nature 1971, 229:542-544.
51. Savageau M. Comparison of classical and autogenous systems of regulation in inducible operons. Nature 1974, 252:546-549.
52. Sekelsky J.J., Newfeld S.J., Raftery L.A., Chartoff E.H., Gelbart W.M. Genetic Characterization and Cloning of Mothers against dpp, a Gene Required for decapentaplegic Function in Drosophila melanogaster. Genetics 1995, 139:1347-1358.
53. Shen-Orr S.S., Milo R., Mangan S., Alon U. Network motifs in the transcriptional regulation network of Escherichia coli. Nat. Genet. 2002, 31:64-68.
54. Smolen P., Baxter D., Byrne J. Mathematical modeling of gene networks. Neuron 2000, 26:567-580.
55. Thieffry D., Huerta A.M., Pérez-Rueda E., Collado-Vides J. From specific gene regulation to genomic networks: a global analysis of transcriptional regulation in Escherichia coli. Bioessays 1998, 20:433-440.
56. Tomoyasu Y., Nakamura M., Ueno N. Role of Dpp signalling in prepattern formation of the dorsocentral mechanosensory organ in Drosophila melanogaster. Development 1998, 125:4215-4224.
57. Tomoyasu Y., Ueno N., Nakamura M. The Decapentaplegic morphogen gradient regulates the notal wingless expression through induction of pannier and u-shaped in Drosophila. Mech. Dev. 2000, 96:37-49.
58. Tsuneizumi K., Nakayama T., Kamoshida Y., Kornberg T., Christian J., Tabata T. Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature 1997, 389:627-631.
59. Wolpert L., Beddington R., Jessell T., Lawrence P., Meyerowitz E., Smith J. Principles of development 2002, Oxford University Press, Oxford.
60. Zeller R., Lopez-Rios J., Zuniga A. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat. Rev. Genet. 2009, 10:845-858.