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Genetics, Vol. 167, 1721-1737, August 2004, Copyright © 2004
doi:10.1534/genetics.104.027334

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Dynamical Analysis of Regulatory Interactions in the Gap Gene System of Drosophila melanogaster

Johannes Jaeger*, Maxim Blagov{dagger}, David Kosman{ddagger}, Konstantin N. Kozlov{dagger}, Manu*, Ekaterina Myasnikova{dagger}, Svetlana Surkova{dagger}, Carlos E. Vanario-Alonso*,§, Maria Samsonova{dagger}, David H. Sharp** and John Reinitz*,1

* Department of Applied Mathematics and Statistics and Center for Developmental Genetics, Stony Brook University, Stony Brook, New York 11794-3600
{dagger} Department of Computational Biology, Center of Advanced Studies, St. Petersburg State Polytechnic University, St. Petersburg, 195251 Russia
{ddagger} Department of Biology, University of California, San Diego, California 92093
§ Universidade Federal do Rio de Janeiro, Instituto de Biofísica Carlos Chagas Filho, Rio de Janeiro, RJ 21949-900, Brazil
** Theoretical Division, Los Alamos National Laboratory, Los Alamos, New Mexico 87545

1 Corresponding author: Department of Applied Mathematics and Statistics, Stony Brook University, Stony Brook, NY 11794-3600.
E-mail: reinitz{at}odd.bio.sunysb.edu

Genetic studies have revealed that segment determination in Drosophila melanogaster is based on hierarchical regulatory interactions among maternal coordinate and zygotic segmentation genes. The gap gene system constitutes the most upstream zygotic layer of this regulatory hierarchy, responsible for the initial interpretation of positional information encoded by maternal gradients. We present a detailed analysis of regulatory interactions involved in gap gene regulation based on gap gene circuits, which are mathematical gene network models used to infer regulatory interactions from quantitative gene expression data. Our models reproduce gap gene expression at high accuracy and temporal resolution. Regulatory interactions found in gap gene circuits provide consistent and sufficient mechanisms for gap gene expression, which largely agree with mechanisms previously inferred from qualitative studies of mutant gene expression patterns. Our models predict activation of Kr by Cad and clarify several other regulatory interactions. Our analysis suggests a central role for repressive feedback loops between complementary gap genes. We observe that repressive interactions among overlapping gap genes show anteroposterior asymmetry with posterior dominance. Finally, our models suggest a correlation between timing of gap domain boundary formation and regulatory contributions from the terminal maternal system.




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