Drosophila melanogaster embryogenesis begins with 13 nuclear division cycles within a syncytium. This produces >6,000 nuclei that, during the next division cycle, become encased in plasma membrane in the process known as cellularization. In this study, we investigate how the secretory membrane system becomes equally apportioned among the thousands of syncytial nuclei in preparation for cellularization. Upon nuclear arrival at the cortex, the endoplasmic reticulum (ER) and Golgi were found to segregate among nuclei, with each nucleus becoming surrounded by a single ER/Golgi membrane system separate from adjacent ones. The nuclear-associated units of ER and Golgi across the syncytial blastoderm produced secretory products that were delivered to the plasma membrane in a spatially restricted fashion across the embryo. This occurred in the absence of plasma membrane boundaries between nuclei and was dependent on centrosome-derived microtubules. The emergence of secretory membranes that compartmentalized around individual nuclei in the syncytial blastoderm is likely to ensure that secretory organelles are equivalently partitioned among nuclei at cellularization and could play an important role in the establishment of localized gene and protein expression patterns within the early embryo.
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24 April 2006
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April 24 2006
The secretory membrane system in the Drosophila syncytial blastoderm embryo exists as functionally compartmentalized units around individual nuclei
David Frescas,
David Frescas
1Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
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Manos Mavrakis,
Manos Mavrakis
1Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
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Holger Lorenz,
Holger Lorenz
1Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
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Robert DeLotto,
Robert DeLotto
2Department of Genetics, Institute of Molecular Biology and Physiology, University of Copenhagen, DK-1353 Copenhagen K, Denmark
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Jennifer Lippincott-Schwartz
Jennifer Lippincott-Schwartz
1Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
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David Frescas
1Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
Manos Mavrakis
1Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
Holger Lorenz
1Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
Robert DeLotto
2Department of Genetics, Institute of Molecular Biology and Physiology, University of Copenhagen, DK-1353 Copenhagen K, Denmark
Jennifer Lippincott-Schwartz
1Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892
Correspondence to Jennifer Lippincott-Schwartz: [email protected]
D. Frescas and M. Mavrakis contributed equally to this paper.
Abbreviations used in this paper: BFA, brefeldin A; FLIP, fluorescence loss in photobleaching; GalT, galactosyltransferase; ROI, region of interest.
Received:
January 27 2006
Accepted:
March 20 2006
Online ISSN: 1540-8140
Print ISSN: 0021-9525
The Rockefeller University Press
2006
J Cell Biol (2006) 173 (2): 219–230.
Article history
Received:
January 27 2006
Accepted:
March 20 2006
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To each nucleus its own ER
Citation
David Frescas, Manos Mavrakis, Holger Lorenz, Robert DeLotto, Jennifer Lippincott-Schwartz; The secretory membrane system in the Drosophila syncytial blastoderm embryo exists as functionally compartmentalized units around individual nuclei . J Cell Biol 24 April 2006; 173 (2): 219–230. doi: https://doi.org/10.1083/jcb.200601156
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