A multiscale investigation of bicoid-dependent transcriptional events in drosophila embryos

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  He, Feng ^a   Ren, Jie ^a,b   Wang, Wei ^a   Ma, Jun ^a  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b Peking University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BICOID MORPHOGENETIC PROTEIN; CYTOKINE; UNCLASSIFIED DRUG; BICOID PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; TRANSACTIVATOR PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; GENE DOSAGE; GENE TARGETING; GENETIC TRANSCRIPTION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; ANIMAL; ANIMAL EMBRYO; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; INTRON; MALE; METABOLISM; PRENATAL DEVELOPMENT;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTRONS; MALE; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 79955537506     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019122     Document Type: Article

References (55)

1. Levine M, Davidson EH, (2005) Gene regulatory networks for development. Proc Natl Acad Sci U S A 102: 4936-4942.
2. Raser JM, O'Shea EK, (2005) Noise in gene expression: origins, consequences, and control. Science 309: 2010-2013.
3. Arias AM, Hayward P, (2006) Filtering transcriptional noise during development: concepts and mechanisms. Nat Rev Genet 7: 34-44.
4. Losick R, Desplan C, (2008) Stochasticity and cell fate. Science 320: 65-68.
5. Driever W, Nusslein-Volhard C, (1988) The bicoid protein determines position in the Drosophila embryo in a concentration-dependent manner. Cell 54: 95-104.
6. Driever W, Nusslein-Volhard C, (1988) A gradient of bicoid protein in Drosophila embryos. Cell 54: 83-93.
7. 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.
8. Struhl G, Struhl K, Macdonald PM, (1989) The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57: 1259-1273.
9. Houchmandzadeh B, Wieschaus E, Leibler S, (2002) Establishment of developmental precision and proportions in the early Drosophila embryo. Nature 415: 798-802.
10. Crauk O, Dostatni N, (2005) Bicoid determines sharp and precise target gene expression in the Drosophila embryo. Curr Biol 15: 1888-1898.
11. Gregor T, Tank DW, Wieschaus EF, Bialek W, (2007) Probing the limits to positional information. Cell 130: 153-164.
12. He F, Wen Y, Deng J, Lin X, Lu LJ, et al. (2008) Probing intrinsic properties of a robust morphogen gradient in Drosophila. Dev Cell 15: 558-567.
13. Lopes FJ, Vieira FM, Holloway DM, Bisch PM, Spirov AV, (2008) Spatial bistability generates hunchback expression sharpness in the Drosophila embryo. PLoS Comput Biol 4: e1000184.
14. Kerszberg M, Wolpert L, (2007) Specifying positional information in the embryo: looking beyond morphogens. Cell 130: 205-209.
15. Lander AD, (2007) Morpheus unbound: reimagining the morphogen gradient. Cell 128: 245-256.
16. Wartlick O, Kicheva A, Gonzalez-Gaitan M, (2009) Morphogen gradient formation. Cold Spring Harb Perspect Biol 1: a001255.
17. 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.
18. Bergmann S, Sandler O, Sberro H, Shnider S, Schejter E, et al. (2007) Pre-steady-state decoding of the Bicoid morphogen gradient. PLoS Biol 5: e46.
19. Ochoa-Espinosa A, Yu D, Tsirigos A, Struffi P, Small S, (2009) Anterior-posterior positional information in the absence of a strong Bicoid gradient. Proc Natl Acad Sci U S A 106: 3823-3828.
20. He F, Saunders TE, Wen Y, Cheung D, Jiao R, et al. (2010) Shaping a morphogen gradient for positional precision. Biophys J 99: 697-707.
21. Manu, Surkova S, Spirov AV, Gursky VV, Janssens H, et al. (2009) Canalization of gene expression in the Drosophila blastoderm by gap gene cross regulation. PLoS Biol 7: e1000049.
22. Tostevin F, ten Wolde PR, Howard M, (2007) Fundamental limits to position determination by concentration gradients. PLoS Comput Biol 3: e78.
23. Okabe-Oho Y, Murakami H, Oho S, Sasai M, (2009) Stable, precise, and reproducible patterning of bicoid and hunchback molecules in the early Drosophila embryo. PLoS Comput Biol 5: e1000486.
24. Erdmann T, Howard M, ten Wolde PR, (2009) Role of spatial averaging in the precision of gene expression patterns. Phys Rev Lett 103: 258101.
25. Gilfillan GD, Dahlsveen IK, Becker PB, (2004) Lifting a chromosome: dosage compensation in Drosophila melanogaster. FEBS Lett 567: 8-14.
26. Gelbart ME, Kuroda MI, (2009) Drosophila dosage compensation: a complex voyage to the X chromosome. Development 136: 1399-1410.
27. Shermoen AW, O'Farrell PH, (1991) Progression of the cell cycle through mitosis leads to abortion of nascent transcripts. Cell 67: 303-310.
28. Wilkie GS, Shermoen AW, O'Farrell PH, Davis I, (1999) Transcribed genes are localized according to chromosomal position within polarized Drosophila embryonic nuclei. Curr Biol 9: 1263-1266.
29. Ronshaugen M, Levine M, (2004) Visualization of trans-homolog enhancer-promoter interactions at the Abd-B Hox locus in the Drosophila embryo. Dev Cell 7: 925-932.
30. Pare A, Lemons D, Kosman D, Beaver W, Freund Y, et al. (2009) Visualization of individual Scr mRNAs during Drosophila embryogenesis yields evidence for transcriptional bursting. Curr Biol 19: 2037-2042.
31. Porcher A, Abu-Arish A, Huart S, Roelens B, Fradin C, et al. (2010) The time to measure positional information: maternal hunchback is required for the synchrony of the Bicoid transcriptional response at the onset of zygotic transcription. Development 137: 2795-2804.
32. Wu YF, Myasnikova E, Reinitz J, (2007) Master equation simulation analysis of immunostained Bicoid morphogen gradient. BMC Syst Biol 1: 52.
33. Gregor T, Wieschaus EF, McGregor AP, Bialek W, Tank DW, (2007) Stability and nuclear dynamics of the bicoid morphogen gradient. Cell 130: 141-152.
34. Ma X, Yuan D, Diepold K, Scarborough T, Ma J, (1996) The Drosophila morphogenetic protein Bicoid binds DNA cooperatively. Development 122: 1195-1206.
35. 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.
36. Abu-Arish A, Porcher A, Czerwonka A, Dostatni N, Fradin C, (2010) High mobility of bicoid captured by fluorescence correlation spectroscopy: implication for the rapid establishment of its gradient. Biophys J 99: L33-35.
37. Mueller F, Wach P, McNally JG, (2008) Evidence for a common mode of transcription factor interaction with chromatin as revealed by improved quantitative fluorescence recovery after photobleaching. Biophys J 94: 3323-3339.
38. Zaidi SK, Young DW, Choi JY, Pratap J, Javed A, et al. (2005) The dynamic organization of gene-regulatory machinery in nuclear microenvironments. EMBO Rep 6: 128-133.
39. Spector DL, (2003) The dynamics of chromosome organization and gene regulation. Annu Rev Biochem 72: 573-608.
40. Hazelrigg T, Liu N, Hong Y, Wang S, (1998) GFP expression in Drosophila tissues: time requirements for formation of a fluorescent product. Dev Biol 199: 245-249.
41. Jackle H, Tautz D, Schuh R, Seifert E, Lehmann R, (1986) Cross-regulatory interactions among the gap genes of Drosophila. Nature 324: 668-670.
42. 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.
43. Lohr U, Chung HR, Beller M, Jackle H, (2009) Antagonistic action of Bicoid and the repressor Capicua determines the spatial limits of Drosophila head gene expression domains. Proc Natl Acad Sci U S A 106: 21695-21700.
44. Hager GL, McNally JG, Misteli T, (2009) Transcription dynamics. Mol Cell 35: 741-753.
45. Ashyraliyev M, Siggens K, Janssens H, Blom J, Akam M, et al. (2009) Gene circuit analysis of the terminal gap gene huckebein. PLoS Comput Biol 5: e1000548.
46. Boettiger AN, Levine M, (2009) Synchronous and stochastic patterns of gene activation in the Drosophila embryo. Science 325: 471-473.
47. Lis JT, (2007) Imaging Drosophila gene activation and polymerase pausing in vivo. Nature 450: 198-202.
48. To TL, Maheshri N, (2010) Noise can induce bimodality in positive transcriptional feedback loops without bistability. Science 327: 1142-1145.
49. Lott SE, Villalta JE, Schroth GP, Luo S, Tonkin LA, et al. (2011) Noncanonical Compensation of Zygotic X Transcription in Early Drosophila melanogaster Development Revealed through Single-Embryo RNA-Seq. PLoS Biol 9: e1000590.
50. Franke A, Dernburg A, Bashaw GJ, Baker BS, (1996) Evidence that MSL-mediated dosage compensation in Drosophila begins at blastoderm. Development 122: 2751-2760.
51. Rastelli L, Richman R, Kuroda MI, (1995) The dosage compensation regulators MLE, MSL-1 and MSL-2 are interdependent since early embryogenesis in Drosophila. Mech Dev 53: 223-233.
52. Smith ER, Allis CD, Lucchesi JC, (2001) Linking global histone acetylation to the transcription enhancement of X-chromosomal genes in Drosophila males. J Biol Chem 276: 31483-31486.
53. He F, Wen Y, Cheung D, Deng J, Lu LJ, et al. (2010) Distance measurements via the morphogen gradient of Bicoid in Drosophila embryos. BMC Dev Biol 10: 80.
54. Liu J, Ma J, (2011) Fates-shifted is an F-box protein that targets Bicoid for degradation and regulates developmental fate determination in Drosophila embryos. Nat Cell Biol 13: 22-29.
55. Gao Q, Finkelstein R, (1998) Targeting gene expression to the head: the Drosophila orthodenticle gene is a direct target of the Bicoid morphogen. Development 125: 4185-4193.