Dynamic network rewiring determines temporal regulatory functions in Drosophila melanogaster development processes

The identification of network motifs has been widely considered as a significant step towards uncovering the design principles of biomolecular regulatory networks. To date, time‐invariant networks have been considered. However, such approaches cannot be used to reveal time‐specific biological traits due to the dynamic nature of biological systems, and hence may not be applicable to development, where temporal regulation of gene expression is an indispensable characteristic. We propose a concept of a “temporal sequence of network motifs”, a sequence of network motifs in active sub‐networks constructed over time, and investigate significant network motifs in the active temporal sub‐networks of Drosophila melanogaster. Based on this concept, we find a temporal sequence of network motifs which changes according to developmental stages and thereby cannot be identified from the whole static network. Moreover, we show that the temporal sequence of network motifs corresponding to each developmental stage can be used to describe pivotal developmental events.

[1]  E. Frise,et al.  Systematic image-driven analysis of the spatial Drosophila embryonic expression landscape , 2010, Molecular systems biology.

[2]  Dmitri A. Papatsenko Stripe formation in the early fly embryo: principles, models, and networks , 2009, Bioessays.

[3]  M. Isalan Gene networks and liar paradoxes , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[4]  Kwang-Hyun Cho,et al.  Hub genes with positive feedbacks function as master switches in developmental gene regulatory networks , 2009, Bioinform..

[5]  Amr Ahmed,et al.  Recovering time-varying networks of dependencies in social and biological studies , 2009, Proceedings of the National Academy of Sciences.

[6]  Chris Mungall,et al.  AmiGO: online access to ontology and annotation data , 2008, Bioinform..

[7]  Kwang-Hyun Cho,et al.  The biphasic behavior of incoherent feed-forward loops in biomolecular regulatory networks. , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

[8]  David Osumi-Sutherland,et al.  FlyBase: enhancing Drosophila Gene Ontology annotations , 2008, Nucleic Acids Res..

[9]  G. Technau,et al.  Antagonistic roles for Ultrabithorax and Antennapedia in regulating segment-specific apoptosis of differentiated motoneurons in the Drosophila embryonic central nervous system , 2008, Development.

[10]  Kwang-Hyun Cho,et al.  Coherent coupling of feedback loops: a design principle of cell signaling networks , 2008, Bioinform..

[11]  W. Mitzner,et al.  Effect of severe calorie restriction on the lung in two strains of mice. , 2008, American journal of physiology. Lung cellular and molecular physiology.

[12]  Anton Crombach,et al.  Evolution of Evolvability in Gene Regulatory Networks , 2008, PLoS Comput. Biol..

[13]  E. Groisman,et al.  Positive feedback in cellular control systems , 2008, BioEssays : news and reviews in molecular, cellular and developmental biology.

[14]  Kwang-Hyun Cho,et al.  Coupled feedback loops form dynamic motifs of cellular networks. , 2008, Biophysical journal.

[15]  Janet M. Thornton,et al.  Evolutionary Models for Formation of Network Motifs and Modularity in the Saccharomyces Transcription Factor Network , 2007, PLoS Comput. Biol..

[16]  Timothy Galitski,et al.  Network motif analysis of a multi-mode genetic-interaction network , 2007, Genome Biology.

[17]  U. Alon Network motifs: theory and experimental approaches , 2007, Nature Reviews Genetics.

[18]  P. Bork,et al.  Identification of tightly regulated groups of genes during Drosophila melanogaster embryogenesis , 2007, Molecular systems biology.

[19]  M. Frasch,et al.  Cardioblast-intrinsic Tinman activity controls proper diversification and differentiation of myocardial cells in Drosophila , 2006, Development.

[20]  G. Lahav,et al.  Cellular Conference Call: External Feedback Affects Cell-Fate Decisions , 2006, Cell.

[21]  B. Kholodenko Cell-signalling dynamics in time and space , 2006, Nature Reviews Molecular Cell Biology.

[22]  Alexander E. Kel,et al.  TRANSFAC® and its module TRANSCompel®: transcriptional gene regulation in eukaryotes , 2005, Nucleic Acids Res..

[23]  Andre Levchenko,et al.  Dynamic Properties of Network Motifs Contribute to Biological Network Organization , 2005, PLoS biology.

[24]  F. Schreiber,et al.  MAVisto: a tool for the exploration of network motifs , 2005, Bioinform..

[25]  R. Amini,et al.  A mechanistic model for quasistatic pulmonary pressure-volume curves for inflation. , 2005, Journal of biomechanical engineering.

[26]  M. Gerstein,et al.  Genomic analysis of regulatory network dynamics reveals large topological changes , 2004, Nature.

[27]  Giacomo Cavalli,et al.  Engrailed and polyhomeotic maintain posterior cell identity through cubitus-interruptus regulation. , 2004, Developmental biology.

[28]  R. Milo,et al.  Network motifs in integrated cellular networks of transcription-regulation and protein-protein interaction. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  S. Shen-Orr,et al.  Superfamilies of Evolved and Designed Networks , 2004, Science.

[30]  Vivek K. Mutalik,et al.  Robust global sensitivity in multiple enzyme cascade system explains how the downstream cascade structure may remain unaffected by cross‐talk , 2004, FEBS letters.

[31]  Sergei Egorov,et al.  Pathway studio - the analysis and navigation of molecular networks , 2003, Bioinform..

[32]  P. R. ten Wolde,et al.  Statistical analysis of the spatial distribution of operons in the transcriptional regulation network of Escherichia coli. , 2003, Journal of molecular biology.

[33]  S. Mangan,et al.  Structure and function of the feed-forward loop network motif , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Dilip Rajagopalan,et al.  A comparison of statistical methods for analysis of high density oligonucleotide array data , 2003, Bioinform..

[35]  H. Jäckle,et al.  FlyMove--a new way to look at development of Drosophila. , 2003, Trends in genetics : TIG.

[36]  Cyrille Alexandre,et al.  Requirements for transcriptional repression and activation by Engrailed in Drosophila embryos , 2003, Development.

[37]  M. Ashburner,et al.  Systematic determination of patterns of gene expression during Drosophila embryogenesis , 2002, Genome Biology.

[38]  S. Shen-Orr,et al.  Network motifs: simple building blocks of complex networks. , 2002, Science.

[39]  Jerry Li,et al.  Within the fold: assessing differential expression measures and reproducibility in microarray assays , 2002, Genome Biology.

[40]  B. S. Baker,et al.  Gene Expression During the Life Cycle of Drosophila melanogaster , 2002, Science.

[41]  F. Beck,et al.  Homeobox genes in gut development , 2002, Gut.

[42]  K. Sneppen,et al.  Specificity and Stability in Topology of Protein Networks , 2002, Science.

[43]  J. Ferrell Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. , 2002, Current opinion in cell biology.

[44]  G. Rubin,et al.  Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Freeman Feedback control of intercellular signalling in development , 2000, Nature.

[46]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[47]  J. Collins,et al.  Construction of a genetic toggle switch in Escherichia coli , 2000, Nature.

[48]  N. Perrimon,et al.  The Transmembrane Molecule Kekkon 1 Acts in a Feedback Loop to Negatively Regulate the Activity of the Drosophila EGF Receptor during Oogenesis , 1999, Cell.

[49]  M. Freeman,et al.  An Autoregulatory Cascade of EGF Receptor Signaling Patterns the Drosophila Egg , 1998, Cell.

[50]  T. L. Jacobsen,et al.  Feedback regulation is central to Delta-Notch signalling required for Drosophila wing vein morphogenesis. , 1997, Development.

[51]  H. Jäckle,et al.  Mechanism and Bicoid‐dependent control of hairy stripe 7 expression in the posterior region of the Drosophila embryo , 1997, The EMBO journal.

[52]  M. Pankratz,et al.  Control of gut development by fork head and cell signaling molecules in Drosophila , 1996, Mechanisms of Development.

[53]  A. Mccarthy Development , 1996, Current Opinion in Neurobiology.

[54]  S. Carroll,et al.  Expression, function, and regulation of the hairy segmentation protein in the Drosophila embryo. , 1988, Genes & development.

[55]  F. Bruggeman,et al.  Introduction to systems biology. , 2007, EXS.

[56]  E. Wingender,et al.  TRANSFAC®: transcriptional regulation, from patterns to profiles , 2003, Nucleic Acids Res..

[57]  G. Morata,et al.  Expression and regulation of the abd-A gene of Drosophila. , 1990, Development.

[58]  L. Wolpert Developmental Biology , 1968, Nature.