The Role of Oocyte Transcription, the 5′UTR, and Translation Repression and Derepression in Drosophila gurken mRNA and Protein Localization

Saunders, Carol J.; Cohen, Robert S.

doi:10.1016/s1097-2765(00)80173-2

Cited by 103 publications

(109 citation statements)

References 54 publications

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“…The anchoring mechanism is not yet clear and is the subject of intense research, but we could envisage that an efficient recruitment of local tER-Golgi units would be achieved by anchoring the mRNA directly on their membrane. The ER was suggested as such an anchor by Saunders and Cohen (1999). Whatever the anchoring mechanism and wherever it is localized, gurken RNA diffuses locally (ϳ20 m; this study), binds to ribosomes, is translated, and recognized by the signal recognition particle that targets it to the most proximal ER membrane, where the protein is synthesized and subsequently transported through the most adjacent tER-Golgi units.…”

Section: It Is Gurken Rna Localization That Dictates the Use Of The Tmentioning

confidence: 80%

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: It Is Gurken Rna Localization That Dictates the Use Of The Tmentioning

confidence: 80%

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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“…MTOC localization to the posterior of stage 2-6 oocytes directs the localization of several cytoplasmic factors to the oocyte posterior cortex, including grk RNA and Grk protein (a TGF-␣ homologue; Fig. 2A; Schupbach, 1993, 1996;Saunders and Cohen, 1999). Grk signaling from the oocyte to the overlying follicle cells at the posterior of the egg chamber specifies those cells to acquire a specific posterior fate (see below).…”

Section: The Posterior Mtoc Directs the Localization Of Cytoplasmic Fmentioning

confidence: 99%

Microtubule polarity and axis formation in theDrosophila oocyte

2006

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The body axes of the fruit fly are established in mid-oogenesis by the localization of three mRNA determinants, bicoid, oskar, and gurken, within the oocyte. General mechanisms of RNA localization and cell polarization, applicable to many cell types, have emerged from investigation of these determinants in Drosophila oogenesis. Localization of these RNAs is dependent on the germline microtubules, which reorganize to form a polarized array at mid-oogenesis in response to a signaling relay between the oocyte and the surrounding somatic follicle cells. Here we describe what is known about this microtubule reorganization and the signaling relay that triggers it. Recent studies have identified a number of ubiquitous RNA binding proteins essential for this process. So far, no targets for any of these proteins have been identified, and future work will be needed to illuminate how they function to reorganize microtubes and whether similar mechanisms also exist in other cell types.

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“…Previous genetic screens based on female sterility and the spindle phenotype also identified DV polarity genes with functions other than DSB repair Wieschaus 1989, 1991;Morris et al 2003;Staeva-Vieira et al 2003). These included genes required for grk mRNA transport (Swan and Suter 1996;Swan et al 1999;Brendza et al 2000;1 Huynh and St Johnston 2000; Navarro et al 2004;Abdu et al 2006), genes required for Grk processing (Styhler et al 1998;Miura et al 2006), and genes regulating the stability and trafficking of Grk protein (Saunders and Cohen 1999;Kennerdell et al 2002;Findley et al 2003;Wilhelm et al 2005;Bokel et al 2006).…”

Section: A S Cells Divide Checkpoints Delay the Transition Tomentioning

confidence: 99%

A Maternal Screen for Genes Regulating Drosophila Oocyte Polarity Uncovers New Steps in Meiotic Progression

2007

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Meiotic checkpoints monitor chromosome status to ensure correct homologous recombination, genomic integrity, and chromosome segregation. In Drosophila, the persistent presence of double-strand DNA breaks (DSB) activates the ATR/Mei-41 checkpoint, delays progression through meiosis, and causes defects in DNA condensation of the oocyte nucleus, the karyosome. Checkpoint activation has also been linked to decreased levels of the TGFa-like molecule Gurken, which controls normal eggshell patterning. We used this easy-toscore eggshell phenotype in a germ-line mosaic screen in Drosophila to identify new genes affecting meiotic progression, DNA condensation, and Gurken signaling. One hundred eighteen new ventralizing mutants on the second chromosome fell into 17 complementation groups. Here we describe the analysis of 8 complementation groups, including Kinesin heavy chain, the SR protein kinase cuaba, the cohesin-related gene dPds5/cohiba, and the Tudor-domain gene montecristo. Our findings challenge the hypothesis that checkpoint activation upon persistent DSBs is exclusively mediated by ATR/Mei-41 kinase and instead reveal a more complex network of interactions that link DSB formation, checkpoint activation, meiotic delay, DNA condensation, and Gurken protein synthesis.

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The Role of Oocyte Transcription, the 5′UTR, and Translation Repression and Derepression in Drosophila gurken mRNA and Protein Localization

Cited by 103 publications

References 54 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 polarity and axis formation in theDrosophila oocyte

A Maternal Screen for Genes Regulating Drosophila Oocyte Polarity Uncovers New Steps in Meiotic Progression

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