Apical Localization of wingless Transcripts Is Required for Wingless Signaling

Simmonds, Andrew; dosSantos, Gilbert; Livne‐Bar, Izhar; Krause, Henry M.

doi:10.1016/s0092-8674(01)00311-7

Cited by 115 publications

(85 citation statements)

References 68 publications

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“…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).…”

Section: Introductionmentioning

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: Introductionmentioning

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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“…29 For example, proper function of the developmental signaling protein Wingless depends upon the apical location of its mRNA. 30 Since Df(3R) how heterozygotes do not dominantly suppress the phenotype of dp ov1 homozygotes, the suppression seen in how 3R-3 heterozygotes must be due to the effects of a mutant protein on Dumpy or its mRNA.…”

Section: Resultsmentioning

confidence: 99%

dumpyinteracts with a large number of genes in the developing wing ofDrosophila melanogaster

Carmon

Topbas²,

Baron³

et al. 2010

Fly

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“…Recent genome-wide screen of RNAs localized in leading edge of migrating mammalian fibroblasts showed that in response to migratory stimuli, 50 different mRNAs (besides previously identified b-actin mRNA) accumulated, via microtubule mediated transport, in the fibroblast protrusions rich in actin cytoskeletal elements (Mili et al, 2008). In epithelial cells, the apical cytoskeleton containing cytokeratin, actin, and microtubules (Salas et al, 1997;Sugimoto et al, 2008) is enriched in localized wingless mRNA (Simmonds et al, 2001;Najand and Simmonds, 2007). In neurons, b-actin mRNA and actin filaments are localized in the growth cones and synapses (Zhang et al, 1999;Specht and Triller, 2008) and a subset of mRNAs localized at the synapse is thought to be responsible for the generation of synaptic plasticity (Kiebler and DesGroseillers, 2000;Czaplinski and Singer, 2006;Bramham and Wells, 2007).…”

Section: Structural Role Of Rna In the Cytoplasm Organization And Maimentioning

confidence: 99%

Teachings from the egg: New and unexpected functions of RNAs

Kloc

2009

Molecular Reproduction Devel

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SUMMARYLocalized mRNAs found in specific regions of somatic cells, germ cells, and embryos function through their protein translation products in cell polarization and development. Recent studies on Xenopus and Drosophila eggs and various somatic cells showed that some of the localized noncoding and coding RNAs play a structural (translation independent) role in maintaining the integrity of microtubule and microfilament cytoskeleton and/or may function in protein folding or as a scaffold for the assembly of cytoplasmic complexes essential for egg or embryo development. In addition, structural noncoding RNAs within the cell nucleus have been shown to be involved in the organization of chromatin, nuclear bodies, and DNA replication. The fact that some of the RNAs may have previously unforeseen structural functions, will change our view on traditional functions of RNAs and will open new frontiers in the field of RNA studies and therapeutic development.Mol. Reprod. Dev. 76: 922-932, 2009. ß

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Apical Localization of wingless Transcripts Is Required for Wingless Signaling

Cited by 115 publications

References 68 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

dumpyinteracts with a large number of genes in the developing wing ofDrosophila melanogaster

Teachings from the egg: New and unexpected functions of RNAs

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