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Precision of Hunchback Expression in the Drosophila Embryo

2012; Elsevier BV; Volume: 22; Issue: 23 Linguagem: Inglês

10.1016/j.cub.2012.09.051

1879-0445

Michael W. Perry, Jacques P. Bothma, Ryan D. Luu, Michael Levine,

Developmental Biology and Gene Regulation

Activation of the gap gene hunchback (hb) by the maternal Bicoid gradient is one of the most intensively studied gene regulatory interactions in animal development. Most efforts to understand this process have focused on the classical Bicoid target enhancer located immediately upstream of the P2 promoter [1Driever W. Nüsslein-Volhard C. The bicoid protein is a positive regulator of hunchback transcription in the early Drosophila embryo.Nature. 1989; 337: 138-143Crossref PubMed Scopus (466) Google Scholar, 2Treisman J. Desplan C. The products of the Drosophila gap genes hunchback and Krüppel bind to the hunchback promoters.Nature. 1989; 341: 335-337Crossref PubMed Scopus (96) Google Scholar, 3Struhl G. Struhl K. Macdonald P.M. The gradient morphogen bicoid is a concentration-dependent transcriptional activator.Cell. 1989; 57: 1259-1273Abstract Full Text PDF PubMed Scopus (450) Google Scholar, 4Houchmandzadeh B. Wieschaus E. Leibler S. Establishment of developmental precision and proportions in the early Drosophila embryo.Nature. 2002; 415: 798-802Crossref PubMed Scopus (391) Google Scholar, 5Porcher A. Abu-Arish A. Huart S. Roelens B. Fradin C. Dostatni N. 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. 2010; 137: 2795-2804Crossref PubMed Scopus (67) Google Scholar, 6Gregor T. Tank D.W. Wieschaus E.F. Bialek W. Probing the limits to positional information.Cell. 2007; 130: 153-164Abstract Full Text Full Text PDF PubMed Scopus (498) Google Scholar, 7Gregor T. Wieschaus E.F. McGregor A.P. Bialek W. Tank D.W. Stability and nuclear dynamics of the bicoid morphogen gradient.Cell. 2007; 130: 141-152Abstract Full Text Full Text PDF PubMed Scopus (369) Google Scholar, 8He F. Wen Y. Deng J. Lin X. Lu L.J. Jiao R. Ma J. Probing intrinsic properties of a robust morphogen gradient in Drosophila.Dev. Cell. 2008; 15: 558-567Abstract Full Text Full Text PDF PubMed Scopus (80) Google Scholar, 9Manu S. Surkova S. Spirov A.V. Gursky V.V. Janssens H. Kim A.R. Radulescu O. Vanario-Alonso C.E. Sharp D.H. Samsonova M. Reinitz J. Canalization of gene expression in the Drosophila blastoderm by gap gene cross regulation.PLoS Biol. 2009; 7: e1000049Crossref PubMed Scopus (211) Google Scholar, 10Holloway D.M. Lopes F.J.P. da Fontoura Costa L. Travençolo B.A.N. Golyandina N. Usevich K. Spirov A.V. Gene expression noise in spatial patterning: hunchback promoter structure affects noise amplitude and distribution in Drosophila segmentation.PLoS Comput. Biol. 2011; 7: e1001069Crossref PubMed Scopus (51) Google Scholar, 11Lopes F.J.P. Vieira F.M.C. Holloway D.M. Bisch P.M. Spirov A.V. Spatial bistability generates hunchback expression sharpness in the Drosophila embryo.PLoS Comput. Biol. 2008; 4: e1000184Crossref PubMed Scopus (52) Google Scholar, 12Manu Surkova S. Spirov A.V. Gursky V.V. Janssens H. Kim A. Radulescu O. Vanario-Alonso C.E. Sharp D.H. Samsonova M. Reinitz J. Canalization of gene expression and domain shifts in the Drosophila blastoderm by dynamical attractors.PLoS Comp Biol. 2009; 5: e1000303Crossref PubMed Scopus (168) Google Scholar]. However, hb is also regulated by a recently identified distal shadow enhancer as well as a neglected "stripe" enhancer, which mediates expression in both central and posterior regions of cellularizing embryos [13Perry M.W. Boettiger A.N. Levine M. Multiple enhancers ensure precision of gap gene-expression patterns in the Drosophila embryo.Proc. Natl. Acad. Sci. USA. 2011; 108: 13570-13575Crossref PubMed Scopus (159) Google Scholar, 14Margolis J.S. Borowsky M.L. Steingrímsson E. Shim C.W. Lengyel J.A. Posakony J.W. Posterior stripe expression of hunchback is driven from two promoters by a common enhancer element.Development. 1995; 121: 3067-3077PubMed Google Scholar]. Here, we employ BAC transgenesis and quantitative imaging methods to investigate the individual contributions of these different enhancers to the dynamic hb expression pattern. These studies reveal that the stripe enhancer is crucial for establishing the definitive border of the anterior Hb expression pattern, just beyond the initial border delineated by Bicoid. Removal of this enhancer impairs dynamic expansion of hb expression and results in variable cuticular defects in the mesothorax (T2) due to abnormal patterns of segmentation gene expression. The stripe enhancer is subject to extensive regulation by gap repressors, including Kruppel, Knirps, and Hb itself. We propose that this repression helps ensure precision of the anterior Hb border in response to variations in the Bicoid gradient.