Spatial bistability generates hunchback expression sharpness in the Drosophila embryo

PLoS Computational Biology

Volumn 4, Issue 9, 2008, Pages

  Lopes, Francisco J P ^a,b,c   Vieira, Fernando M C ^c,d   Holloway, David M ^e,f,g   Bisch, Paulo M ^c   Spirov, Alexander V ^a,b  

^a Stony Brook University   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d UNIVERSITY OF BRASILIA   (Brazil)

^e BRITISH COLUMBIA INSTITUTE OF TECHNOLOGY   (Canada)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^g UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; EIGENVALUES AND EIGENFUNCTIONS; GENE EXPRESSION REGULATION; PROTEINS;

CONCENTRATION- GRADIENTS; COOPERATIVE BINDING; DROSOPHILA EMBRYOS; EMBRYONIC DEVELOPMENT; GENES EXPRESSION; MULTIPLE BINDING SITES; PATTERN FORMATION; POSITIONAL INFORMATION; SELF REGULATION; SPATIAL BISTABILITY;

TRANSCRIPTION;

BETA GALACTOSIDASE; DNA; MESSENGER RNA; BICOID PROTEIN, DROSOPHILA; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; HUNCHBACK PROTEIN, DROSOPHILA; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; DNA BINDING; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO DEVELOPMENT; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOTYPE; HUNCHBACK GENE; IMAGE PROCESSING; MODEL; MUTANT; NONHUMAN; PROTEIN EXPRESSION; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; MORPHOGENESIS; MUTATION; PRENATAL DEVELOPMENT;

DROSOPHILA MELANOGASTER;

ANIMALS; BINDING SITES; BODY PATTERNING; COMPUTATIONAL BIOLOGY; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENES, INSECT; GENOTYPE; HOMEODOMAIN PROTEINS; MODELS, GENETIC; MUTATION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 52949139446     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000184     Document Type: Article

References (84)

1. Driesch H (1893) Entwicklungsmechanische studien VI. Über einige fragen der theoretischen morphologie. Z Wiss Zool 55: 34-62.
2. Browne EN (1909) The production of new hydranths in hydra by the insertion of small grafts. J Exp Zool 7: 1-37.
3. Wolpert L (1969) Positional information and spatial pattern of cellular differentiation. J Theor Biol 25: 1-47.
4. Lander AD (2007) Morpheus unbound: reimagining the morphogen gradient. Cell 128: 245-256.
5. Lander AD, Nie Q, Wan FYM (2002) Do morphogen gradients arise by diffusion? Dev Biol 247: 471-471.
6. Gregor T, Bialek W, van Steveninck RRR, Tank DW, Wieschaus EF (2005) Diffusion and scaling during early embryonic pattern formation. Proc Natl Acad Sci U S A 102: 18403-18407.
7. Driever W, Nüsslein-Volhard C (1988) The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54: 95-104.
8. Driever W, Nüsslein-Volhard C (1988) A gradient of bicoid protein in Drosophila embryos. Cell 54: 83-93.
9. Struhl G, Struhl K, Macdonald PM (1989) The gradient morphogen Bicoid is a concentration-dependent transcriptional activator. Cell 57: 1259-1273.
10. Wolpert L (2002) Principles of Development. 2nd ed. New York: Oxford University Press.
11. Ephrussi A, St Johnston D (2004) Seeing is believing: the bicoid morphogen gradient matures. Cell 116: 143-152.
12. Bonn D, Meunier J, Greffier O, Al-Kahwaji A, Kellay H (1998) Bistability in non-Newtonian flow: rheology of lyotropic liquid crystals. Phys Rev E 58: 2115-2118.
13. Sessoli R, Gatteschi D, Caneschi A, Novak MA (1993) Magnetic bistability in a metal-ion cluster. Nature 365: 141-143.
14. Bhalla US, Iyengar R (1999) Emergent properties of networks of biological signaling pathways. Science 283: 381-387.
15. Vieira FMC, Bisch PM (1994) Oscillations and multiple steady-states in active membrane-transport models. Eur Biophys J 23: 277-287.
16. Guidi GM, Goldbeter A (2000) Oscillations and bistability predicted by a model for a cyclical bienzymatic system involving the regulated isocitrate dehydrogenase reaction. Biophys Chem 83: 153-170.
17. Feinberg M, Horn FJM (1974) Dynamics of open chemical systems and algebraic structure of underlying reaction network. Chem Eng Sci 29: 775-787.
18. Leloup JC, Goldbeter A (1998) A model for circadian rhythms in Drosophila incorporating the formation of a complex between the PER and TIM proteins. J Biol Rhythms 13: 70-87.
19. Calzone L, Thieffry D, Tyson JJ, Novak B (2007) Dynamical modeling of syncytial mitotic cycles in Drosophila embryos. Mol Syst Biol 3: 131.
20. Kim J, White KS, Winfree E (2006) Construction of an in vitro bistable circuit from synthetic transcriptional switches. Mol Syst Biol 2: 68.
21. Umulis DM, Serpe M, O'Connor MB, Othmer HG (2006) Robust, bistable patterning of the dorsal surface of the Drosophila embryo. Proc Natl Acad Sci U S A 103: 11613-11618.
22. Wang YC, Ferguson EL (2005) Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434: 229-234.
23. Nussleinvolhard C, Frohnhofer HG, Lehmann R (1987) Determination of anteroposterior polarity in Drosophila. Science 238: 1675-1681.
24. Berleth T, Burri M, Thoma G, Bopp D, Richstein S, et al. (1988) The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J 7: 1749-1756.
25. Jäckle H, Tautz D, Schuh R, Seifert E, Lehmann R (1986) Cross-regulatory interactions among the gap genes of Drosophila. Nature 324: 668-670.
26. Frohnhofer HG, Nussleinvolhard C (1986) Organization of anterior pattern in the Drosophila embryo by the maternal gene bicoid. Nature 324: 120-125.
27. Struhl G (1989) Differing strategies for organizing anterior and posterior body pattern in Drosophila embryos. Nature 338: 741-744.
28. Nüsslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287: 795-801.
29. Holloway DM, Harrison LG, Kosman D, Vanario-Alonso CE, Spirov AV (2006) Analysis of pattern precision shows that Drosophila segmentation develops substantial independence from gradients of maternal gene products. Dev Dyn 235: 2949-2960.
30. Spirov AV, Holloway DM (2003) Making the body plan: precision in the genetic hierarchy of Drosophila embryo segmentation. In Silico Biol 3: 89-100.
31. Jaeger J, Surkova S, Blagov M, Janssens H, Kosman D, et al. (2004) Dynamic control of positional information in the early Drosophila embryo. Nature 430: 368-371.
32. von Dassow G, Meir E, Munro EM, Odell GM (2000) The segment polarity network is a robust development module. Nature 406: 188-192.
33. Tautz D, Lehmann R, Schnurch H, Schuh R, Seifert E, et al. (1987) Finger protein of novel structure encoded by Hunchback, a 2nd member of the gap class of Drosophila segmentation genes. Nature 327: 383-389.
34. Driever W, Nusslein-Volhard C (1989) The Bicoid protein is a positive regulator of Hunchback transcription in the early Drosophila embryo. Nature 337: 138-143.
35. Treisman J, Desplan C (1989) The products of the Drosophila gap genes Hunchback and krüppel bind to the Hunchback promoters. Nature 341: 335-337.
36. Margolis JS, Borowsky ML, Steingrimsson E, Shim GW, Lengyel JA, et al. (1995) Posterior stripe expression of Hunchback is driven from 2 promoters by a common enhancer element. Development 121: 3067-3077.
37. Lukowitz W, Schroder C, Glaser G, Hulskamp M, Tautz D (1994) Regulatory and coding regions of the segmentation gene Hunchback are functionally conserved between Drosophila-virilis and Drosophila-melanogaster. Mech Dev 45: 105-115.
38. Wu XL, Vasisht V, Kosman D, Reinitz J, Small S (2001) Thoracic patterning by the Drosophila gap gene hunchback. Dev Biol 237: 79-92.
39. Simpsonbrose M, Treisman J, Desplan C (1994) Synergy between the Hunchback and Bicoid morphogens is required for anterior patterning in Drosophila. Cell 78: 855-865.
40. Struhl G, Johnston P, Lawrence PA (1992) Control of Drosophila body pattern by the Hunchback morphogen gradient. Cell 69: 237-249.
41. Wimmer EA, Carleton A, Harjes P, Turner T, Desplan C (2000) Bicoid-independent formation of thoracic segments in Drosophila. Science 287: 2476-2479.
42. Lehmann R, Nussleinvolhard C (1987) Hunchback, a gene required for segmentation of an anterior and posterior region of the Drosophila embryo. Dev Biol 119: 402-417.
43. Driever W, Thoma G, Nusslein-Volhard C (1989) Determination of spatial domains of zygotic gene-expression in the Drosophila embryo by the affinity of binding-sites for the Bicoid morphogen. Nature 340: 363-367.
44. Ma XG, Yuan D, Diepold K, Scarborough T, Ma J (1996) The Drosophila morphogenetic protein Bicoid binds DNA cooperatively. Development 122: 1195-1206.
45. Lopes FJP, Vanario-Alonso CE, Bisch PM, Vieira FMC (2005) A kinetic mechanism for Drosophila Bicoid cooperative binding. J Theor Biol 235: 185-198.
46. Lebrecht D, Foehr M, Smith E, Lopes FJP, Vanario-Alonso CE, et al. (2005) Bicoid cooperative DNA binding is critical for embryonic patterning in Drosophila. Proc Natl Acad Sci U S A 102: 13176-13181.
47. Burz DS, Rivera-Pomar R, Jackle H, Hanes SD (1998) Cooperative DNA-binding by Bicoid provides a mechanism for threshold-dependent gene activation in the Drosophila embryo. EMBO J 17: 5998-6009.
48. Gregor T, Tank DW, Wieschaus EF, Bialek W (2007) Probing the limits to positional information. Cell 130: 153-164.
49. Crauk O, Dostatni N (2005) Bicoid determines sharp and precise target gene expression on the Drosophila embryo. Curr Biol 15: 1888-1898.
50. Houchmandzadeh B, Wieschaus E, Leibler S (2002) Establishment of developmental precision and proportions in the early Drosophila embryo. Nature 415: 798-802.
51. Simpson-Brose M, Treisman J, Desplan C (1994) Synergy between the Hunchback and Bicoid morphogens is required for anterior patterning in Drosophila. Cell 78: 855-865.
52. Hülskamp M, Lukowitz W, Beermann A, Glaser G, Tautz D (1994) Differential regulation of target genes by different alleles of the segmentation gene Hunchback in Drosophila. Genetics 138: 125-134.
53. Schroder C, Tautz D, Seifert E, Jackle H (1988) Differential regulation of the 2 transcripts from the Drosophila gap segmentation gene Hunchback. EMBO J 7: 2881-2887.
54. Burz DS, Hanes SD (2001) Isolation of mutations that disrupt cooperative DNA binding by the Drosophila Bicoid protein. J Mol Biol 305: 219-230.
55. Horn F, Jackson R (1972) General mass action kinetics. Arch Ration Mech Anal 47: 81-116.
56. Li HY (1998) Zero eigenvalue analysis for the determination of multiple steady states in reaction networks. Z Naturforsch [A] 53: 171-177.
57. Li HY (1999) Determination of multiple steady states in an active membrane transport model. Z Naturforsch [A] 54: 245-250.
58. Li HY (1998) Determination of multiple steady states in a family of allosteric models for glycolysis. J Chem Phys 109: 8485-8493.
59. Chuang GS, Chao AC, Ho PY, Li HY (2004) Computational multiple steady states in enzymatically catalyzed oxidation of monophenols by tyrosinase in an isothermal CFSTR. Biochem Eng J 21: 161-170.
60. Lopes FJP (2002) Analise da Formacao de Padroes no Desenvolvimento da Drosophila melanogaster atraves de Modelos de Redes Complexas [PhD thesis]. Rio de Janeiro: Universidade Federal do Rio de Janeiro.
61. Gregor T, Wieschaus EF, McGregor AP, Bialek W, Tank DW (2007) Stability and nuclear dynamics of the bicoid morphogen gradient. Cell 130: 141-152.
62. Isshiki T, Pearson B, Holbrook S, Doe CQ (2001) Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106: 511-521.
63. Merrill PT, Sweeton D, Wieschaus E (1988) Requirements for autosomal gene activity during precellular stages of Drosophila-melanogaster. Development 104: 495-509.
64. Tautz D (1988) Regulation of the Drosophila segmentation gene Hunchback by 2 maternal morphogenetic centers. Nature 332: 281-284.
65. Hulskamp M, Schroder C, Pfeifle C, Jackle H, Tautz D (1989) Posterior segmentation of the drosophila embryo in the absence of a maternal posterior organizer gene. Nature 338: 629-632.
66. Irish V, Lehmann R, Akam M (1989) The Drosophila posterior-group gene Nanos functions by repressing Hunchback activity. Nature 338: 646-648.
67. Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene Hunchback. Chromosoma 98: 81-85.
68. Wang C, Lehmann R (1991) Nanos is the localized posterior determinant in Drosophila. Cell 66: 637-647.
69. Wharton RP, Struhl G (1991) RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen Nanos. Cell 67: 955-967.
70. Horn F (1972) Necessary and sufficient conditions for complex balancing in chemical-kinetics. Arch Ration Mech Anal 49: 172-186.
71. Feinberg M (1987) Chemical-reaction network structure and the stability of complex isothermal reactors. 1. The deficiency-zero and deficiency-one theorems. Chem Eng Sci 42: 2229-2268.
72. Craciun G, Feinberg M (2005) Multiple equilibria in complex chemical reaction networks: I. The injectivity property. SIAM J Appl Math 65: 1526-1546.
73. Li HY, Ho PY (2000) Subnetwork analysis for the determination of multiple steady states in complex reaction networks. Ind Eng Chem Res 39: 3291-3297.
74. Lewis J, Slack JMW, Wolpert L (1977) Thresholds in development. J Theor Biol 65: 579-590.
75. Ingolia NT (2004) Topology and robustness in the Drosophila segment polarity network. Plos Biol 2: e123. doi:10.1371/journal.pbio.0020123.
76. Janssens H (2005) A high-throughput method for quantifying gene expression data from early Drosophila embryos. Dev Genes Evol 215: 374-381.
77. Poustelnikova E, Pisarev A, Blagov M, Samsonova M, Reinitz J (2004) A database for management of gene expression data in situ. Bioinformatics 20: 2212-2221.
78. Moodley K, Murrell H (2004) A colour-map plugin for the open source, Java based, image processing package, ImageJ. Comput Geosci 30: 609-618.
79. Tsonis AA, Kumar P, Elsner JB, Tsonis PA (1996) Wavelet analysis of DNA sequences. Phys Rev E 53: 1828-1834.
80. Golyandina N, Nekrutkin VV, Zhigliavskiǐ A (2001) Analysis of Time Series Structure: SSA and Related Techniques. Boca Raton (Florida): Chapman & Hall/CRC.
81. Alexandrov T, Golyandina N, Spirov A (2008) Singular spectrum analysis of gene expression profiles of early Drosophila embryo: exponential-in-distance patterns. Res Lett Signal Process 2008: 5.
82. Myasnikova E, Samsonova M, Kosman D, Reinitz J (2005) Removal of background signal from in situ data on the expression of segmentation genes in Drosophila. Dev Genes Evol 215: 320-326.
83. Fuks DB, Tabachnikov S (2007) Mathematical Omnibus: Thirty Lectures on Classic Mathematics. Providence (Rhode Island): American Mathematical Society.
84. Goldbete A, Lefever R (1972) Dissipative structures for an allosteric model-Application to glycolytic oscillations. Biophys J 12: 1302-1315.