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Bicoid gradient formation mechanism and dynamics revealed by protein lifetime analysis

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Durrieu, Lucia, Kirrmaier, Daniel, Schneidt, Tatjana, Kats, Ilia, Raghavan, Sarada, Hufnagel, Lars, Saunders, Timothy E. and Knop, Michael (2018) Bicoid gradient formation mechanism and dynamics revealed by protein lifetime analysis. Molecular Systems Biology, 14 (9). e8355. doi:10.15252/msb.20188355

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Official URL: http://dx.doi.org/10.15252/msb.20188355

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Abstract

Embryogenesis relies on instructions provided by spatially organized signaling molecules known as morphogens. Understanding the principles behind morphogen distribution and how cells interpret locally this information remains a major challenge in developmental biology. Here, we introduce morphogen‐age measurements as a novel approach to test models of morphogen gradient formation. Using a tandem fluorescent timer as a protein age sensor, we find a gradient of increasing age of Bicoid along the anterior–posterior axis in the early Drosophila embryo. Quantitative analysis of the protein age distribution across the embryo reveals that the synthesis–diffusion–degradation model is the most likely model underlying Bicoid gradient formation, and rules out other hypotheses for gradient formation. Moreover, we show that the timer can detect transitions in the dynamics associated with syncytial cellularization. Our results provide new insight into Bicoid gradient formation and demonstrate how morphogen‐age information can complement knowledge about movement, abundance, and distribution, which should be widely applicable to other systems.

Item Type: Journal Article
Subjects: Q Science > QH Natural history > QH301 Biology
Q Science > QL Zoology
Divisions: Faculty of Medicine > Warwick Medical School > Biomedical Sciences
Faculty of Medicine > Warwick Medical School
Library of Congress Subject Headings (LCSH): Drosophila melanogaster, Embryology, Biological systems -- Research, Developmental biology
Journal or Publication Title: Molecular Systems Biology
Publisher: Nature Publishing Group
ISSN: 1744-4292
Official Date: 2018
Dates:
DateEvent
2018Published
Volume: 14
Number: 9
Article Number: e8355
DOI: 10.15252/msb.20188355
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
UNSPECIFIEDEuropean Molecular Biology Laboratoryhttp://dx.doi.org/10.13039/100013060
EIPODEuropean Molecular Biology Laboratoryhttp://dx.doi.org/10.13039/100013060
UNSPECIFIEDKavli Institute for Theoretical Physics, University of California, Santa Barbarahttp://dx.doi.org/10.13039/100005956
FellowshipNational Research Foundation Singaporehttp://dx.doi.org/10.13039/501100001381
EcTop2[DFG] Deutsche Forschungsgemeinschafthttp://dx.doi.org/10.13039/501100001659
EcTop2Universität Heidelberghttp://viaf.org/viaf/155544909
INST 35/1314-1 FUGG[DFG] Deutsche Forschungsgemeinschafthttp://dx.doi.org/10.13039/501100001659

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