The Drosophila TGF-α-like protein Gurken: expression and cellular localization during Drosophila oogenesis

Neuman-Silberberg, F. Shira; Schüpbach, Trudi

doi:10.1016/0925-4773(96)00567-9

Cited by 164 publications

(102 citation statements)

References 29 publications

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“…Gurken protein exhibits a restricted and polar localization at the D/A corner of a stage 9 -10 oocyte (Neuman-Silberberg et al, 1996). The tER-Golgi units that make up the oocyte exocytic pathway are evenly distributed.…”

Section: Gurken Protein Is Only Transported Through the Tergolgi Unitmentioning

confidence: 99%

mRNA Localization and ER-based Protein Sorting Mechanisms Dictate the Use of Transitional Endoplasmic Reticulum-Golgi Units Involved in Gurken Transport inDrosophilaOocytes

Herpers

Rabouille

2004

MBoC

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The anteroposterior and dorsoventral axes of the future embryo are specified within Drosophila oocytes by localizing gurken mRNA, which targets the secreted Gurken transforming growth factor-␣ synthesis and transport to the same site. A key question is whether gurken mRNA is targeted to a specialized exocytic pathway to achieve the polar deposition of the protein. Here, we show, by (immuno)electron microscopy that the exocytic pathway in stage 9 -10 Drosophila oocytes comprises a thousand evenly distributed transitional endoplasmic reticulum (tER)-Golgi units. Using Drosophila mutants, we show that it is the localization of gurken mRNA coupled to efficient sorting of Gurken out of the ER that determines which of the numerous equivalent tER-Golgi units are used for the protein transport and processing. The choice of tER-Golgi units by mRNA localization makes them independent of each other and represents a nonconventional way, by which the oocyte implements polarized deposition of transmembrane/secreted proteins. We propose that this pretranslational mechanism could be a general way for targeted secretion in polarized cells, such as neurons. INTRODUCTIONPolarized localization of proteins is achieved by at least two different mechanisms. The first one relies on restricted localization of mRNAs that encode cytosolic proteins, allowing local protein translation, thus creating differential protein activity and generating cell asymmetry and polarity (Bashirullah et al., 1998). This is, for instance, the case of actin mRNA localization in the nerve terminal of neurons (Lee and Hollenbeck, 2003), oskar localization at the posterior pole of Drosophila oocytes (Ephrussi et al., 1991), and ash1 localization in dividing yeast cells (Long et al., 1997). On the other hand, the mechanism ensuring the polarized deposition of transmembrane or secreted proteins is thought, in mammalian cells, to be achieved by posttranslational sorting events in the trans-Golgi network (TGN). There, signals in their cytoplasmic tail or lumenal domain are deciphered, resulting in the directed movement of specialized transport vesicles to allow specific deposition at the apical or basolateral plasma membrane of epithelial cells (Ikonen and Simons, 1998;Nelson and Yeaman, 2001).However, there is a growing number of transmembrane and secreted proteins for which their transcript also exhibits a restricted localization. The transcript for the yeast plasma membrane protein Ist2 is actively transported along the acto-myosin network to the bud tip (Takizawa et al., 2000), and the protein is deposited locally (Juschke et al., 2004). wingless mRNA is localized apically in epithelial cells (Simmonds et al., 2001). In a stage 9 -10 Drosophila oocytes, gurken mRNA is transported and deposited exclusively in the dorsal/anterior corner (D/A; Neuman-Silberberg and Schupbach, 1993; Figure 1B). gurken encodes a protein that is synthesized in the endoplasmic reticulum (ER) as a 285-amino acid type I transmembrane protein precursor and transported to the Golgi apparat...

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Section: Gurken Protein Is Only Transported Through the Tergolgi Unitmentioning

confidence: 99%

mRNA Localization and ER-based Protein Sorting Mechanisms Dictate the Use of Transitional Endoplasmic Reticulum-Golgi Units Involved in Gurken Transport inDrosophilaOocytes

Herpers

Rabouille

2004

MBoC

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“…Besides anterior-posterior axis determination, dorsal-ventral patterning in Drosophila embryos is prespecified by the asymmetry of the oocyte (42). The oocyte nucleus becomes localized to the anterodorsal corner, and nucleus-associated gurken mRNA localization and translation define the dorsal-ventral axis by determining dorsal cell fates in lateral follicle cells (42,(44)(45)(46)(47)(48). KHC has been shown to be required for the proper nucleus position, and thus dorsal-ventral patterning (49), although the mechanism is not well understood.…”

Section: Sliding Between Cortically Anchored Microtubules and Free Cymentioning

confidence: 99%

Microtubule–microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes

Lü

Winding

Lakonishok

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

122

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Cytoplasmic streaming in Drosophila oocytes is a microtubulebased bulk cytoplasmic movement. Streaming efficiently circulates and localizes mRNAs and proteins deposited by the nurse cells across the oocyte. This movement is driven by kinesin-1, a major microtubule motor. Recently, we have shown that kinesin-1 heavy chain (KHC) can transport one microtubule on another microtubule, thus driving microtubule-microtubule sliding in multiple cell types. To study the role of microtubule sliding in oocyte cytoplasmic streaming, we used a Khc mutant that is deficient in microtubule sliding but able to transport a majority of cargoes. We demonstrated that streaming is reduced by genomic replacement of wild-type Khc with this sliding-deficient mutant. Streaming can be fully rescued by wild-type KHC and partially rescued by a chimeric motor that cannot move organelles but is active in microtubule sliding. Consistent with these data, we identified two populations of microtubules in fast-streaming oocytes: a network of stable microtubules anchored to the actin cortex and free cytoplasmic microtubules that moved in the ooplasm. We further demonstrated that the reduced streaming in sliding-deficient oocytes resulted in posterior determination defects. Together, we propose that kinesin-1 slides free cytoplasmic microtubules against cortically immobilized microtubules, generating forces that contribute to cytoplasmic streaming and are essential for the refinement of posterior determinants.kinesin-1 | microtubules | cytoplasmic streaming | Drosophila | axis determination

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“…DV asymmetry within the follicular epithelium is established during mid-oogenesis by the product of the gurken (grk) gene, a transforming growth factor (TGF) ␣-like molecule restricted to the future dorsal side of the oocyte (Neuman-Silberberg and Schübach, 1993;Neuman-Silberberg and Schübach, 1996). Grk acts as a localized ligand for the Drosophila epidermal growth factor receptor (Egfr) in the overlying follicle cells, and the resulting localized Egfr activity defines the dorsal region of the epithelium (Nilson and Schübach, 1999;Roth, 2003;Van Buskirk and Schübach, 1999).…”

Section: Introductionmentioning

confidence: 99%

Capicua regulates follicle cell fate in theDrosophilaovary through repression ofmirror

et al. 2006

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The dorsoventral axis of the Drosophila egg is established by dorsally localized activation of the epidermal growth factor receptor (Egfr)in the ovarian follicular epithelium. Subsequent positive- and negative-feedback regulation generates two dorsolateral follicle cell primordia that will produce the eggshell appendages. A dorsal midline domain of low Egfr activity between the appendage primordia defines their dorsal boundary, but little is known about the mechanisms that establish their ventral limit. We demonstrate that the transcriptional repressor Capicua is required cell autonomously in ventral and lateral follicle cells to repress dorsal fates, and functions in this process through the repression of mirror. Interestingly, ectopic expression of mirror in the absence of capicua is observed only in the anterior half of the epithelium. We propose that Capicua regulates the pattern of follicle cell fates along the dorsoventral axis by blocking the induction of appendage determinants, such as mirror, by anterior positional cues.

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The Drosophila TGF-α-like protein Gurken: expression and cellular localization during Drosophila oogenesis

Cited by 164 publications

References 29 publications

mRNA Localization and ER-based Protein Sorting Mechanisms Dictate the Use of Transitional Endoplasmic Reticulum-Golgi Units Involved in Gurken Transport inDrosophilaOocytes

mRNA Localization and ER-based Protein Sorting Mechanisms Dictate the Use of Transitional Endoplasmic Reticulum-Golgi Units Involved in Gurken Transport inDrosophilaOocytes

Microtubule–microtubule sliding by kinesin-1 is essential for normal cytoplasmic streaming in Drosophila oocytes

Capicua regulates follicle cell fate in theDrosophilaovary through repression ofmirror

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