» Articles » PMID: 16636144

The Secretory Membrane System in the Drosophila Syncytial Blastoderm Embryo Exists As Functionally Compartmentalized Units Around Individual Nuclei

Overview
Journal J Cell Biol
Specialty Cell Biology
Date 2006 Apr 26
PMID 16636144
Citations 49
Authors
Affiliations
Soon will be listed here.
Abstract

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.

Citing Articles

Centrosome-organized plasma membrane infoldings linked to growth of a cortical actin domain.

Tam R, Harris T J Cell Biol. 2024; 223(10).

PMID: 38935075 PMC: 11215285. DOI: 10.1083/jcb.202403115.


Reshaping the Syncytial Drosophila Embryo with Cortical Actin Networks: Four Main Steps of Early Development.

Tam R, Harris T Results Probl Cell Differ. 2023; 71:67-90.

PMID: 37996673 DOI: 10.1007/978-3-031-37936-9_4.


Dysregulation of the endoplasmic reticulum blocks recruitment of centrosome-associated proteins resulting in mitotic failure.

Rollins K, Blankenship J Development. 2023; 150(22).

PMID: 37971218 PMC: 10690056. DOI: 10.1242/dev.201917.


Proteins rather than mRNAs regulate nucleation and persistence of Oskar germ granules in Drosophila.

Curnutte H, Lan X, Sargen M, Ao Ieong S, Campbell D, Kim H Cell Rep. 2023; 42(7):112723.

PMID: 37384531 PMC: 10439980. DOI: 10.1016/j.celrep.2023.112723.


Endoplasmic reticulum membranes are continuously required to maintain mitotic spindle size and forces.

Araujo M, Tavares A, Vieira D, Telley I, Oliveira R Life Sci Alliance. 2022; 6(1).

PMID: 36379670 PMC: 9671068. DOI: 10.26508/lsa.202201540.


References
1.
Pritchard D, Schubiger G . Activation of transcription in Drosophila embryos is a gradual process mediated by the nucleocytoplasmic ratio. Genes Dev. 1996; 10(9):1131-42. DOI: 10.1101/gad.10.9.1131. View

2.
Smith C, DeLotto R . Ventralizing signal determined by protease activation in Drosophila embryogenesis. Nature. 1994; 368(6471):548-51. DOI: 10.1038/368548a0. View

3.
Terasaki M, Runft L, Hand A . Changes in organization of the endoplasmic reticulum during Xenopus oocyte maturation and activation. Mol Biol Cell. 2001; 12(4):1103-16. PMC: 32290. DOI: 10.1091/mbc.12.4.1103. View

4.
Terasaki M . Dynamics of the endoplasmic reticulum and golgi apparatus during early sea urchin development. Mol Biol Cell. 2000; 11(3):897-914. PMC: 14819. DOI: 10.1091/mbc.11.3.897. View

5.
Foe V, Alberts B . Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci. 1983; 61:31-70. DOI: 10.1242/jcs.61.1.31. View