The drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGFα-like protein

Neuman-Silberberg, F. Shira; Schüpbach, Trudi

doi:10.1016/s0092-8674(05)80093-5

Cited by 491 publications

(247 citation statements)

References 62 publications

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“…Mutant fly stocks used are dCOG5-GFP (w;GFP-Fws/Cyo) (Farkas et al, 2003); PDI-GFP (PDI::GFP/GFP-TM3,Sb) (Bobinnec et al, 2003) (Norvell et al, 1999); cni AR55 (b cni AR55 pr cn/Cyo), cni CF5 (b cni CF5 pr cn wx bw/Cyo) and cni AA12 (b cni AA12 /Cyo) (Roth et al, 1995); grk 2B6 (grk[2B6]b cn s L bo/Cyo) and grk 2E12 (w; grk[2E12]b/Cyo) (Neuman-Silberberg and Schupbach, 1993); and fly lines expressing Gurken lacking the transmembrane and the cytoplasmic domain g⌬TC4.1 and the cytoplasmic domain g⌬C100 (Queenan et al, 1999). The stocks carrying the constructs encoding the truncated versions of Gurken proteins were crossed into the grk 2B6 background and females from this cross were mated with male grk 2E12 to yield orange-eyed black flies (g⌬TC4.1; grk 2B6 /grk 2E12 and g⌬C100; grk 2B6 /grk 2E12 ).…”

Section: Fly Stocksmentioning

confidence: 99%

“…Digoxigenin-labeled gurken RNAprobe was produced from the 1.7-kb gurken cDNA (Neuman-Silberberg and Schupbach, 1993) by using a DIG RNA labeling kit according to manufacturer's recommendations (Roche Diagnostics, Mannheim, Germany).…”

Section: In Situ Hybridizationmentioning

confidence: 99%

“…(Neuman-Silberberg and Schupbach, 1993); and fly lines expressing Gurken lacking the transmembrane and the cytoplasmic domain g⌬TC4.1 and the cytoplasmic domain g⌬C100 (Queenan et al, 1999). The stocks carrying the constructs encoding the truncated versions of Gurken proteins were crossed into the grk 2B6 background and females from this cross were mated with male grk 2E12 to yield orange-eyed black flies (g⌬TC4.1; grk 2B6 /grk 2E12 and g⌬C100; grk 2B6 /grk 2E12 ).…”

Section: Introductionmentioning

confidence: 99%

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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: Fly Stocksmentioning

confidence: 99%

Section: In Situ Hybridizationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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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 Drosophila vasa gene encodes a DEAD-box protein with ATP-dependent RNA-helicase activity (Hay et al, 1988;Lasko and Ashburner 1988). The helicase activity is required for the translation of at least two mRNAs involved in germ cell migration and development, ie, nanos (Forbes and Lehmann 1998;Gavis et al, 1996;Kobayashi et al, 1996) and gurken (Gonzalez-Reyes et al, 1995;Neuman-Silberberg and Schupbach 1993;Roth et al, 1995;Styhler et al, 1998;Tomancak et al, 1998). VASA is present in the developing oocyte and is part of the germ plasm, a poorly understood ribonucleoprotein complex crucial for germ cell determination.…”

mentioning

confidence: 99%

VASA Is a Specific Marker for Both Normal and Malignant Human Germ Cells

Zeeman

Stoop

Boter

et al. 2002

Laboratory Investigation

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SUMMARY:VASA is so far the only known gene in mammals whose expression is specific for the germ cell lineage. We investigated the presence of VASA mRNA and protein in a series of germ cell tumors of different histologic subtypes and anatomic location, as well as in nongerm cell tumors such as testicular lymphomas and Leydig cell tumors. We detected VASA mRNA (by quantitative RT-PCR) and protein (by immunohistochemical staining) in normal spermatogenesis, seminoma (both classic and spermatocytic), carcinoma in situ (the precursor of classic seminoma and nonseminoma), dysgerminoma, and gonadoblastoma. VASA immunostaining was relatively weak in seminomas and dysgerminomas compared with spermatocytic seminomas, despite similar mRNA levels, suggesting that VASA is regulated in part by post-transcriptional mechanisms. A higher staining intensity compared with the invasive counterparts was observed in the precursor lesions (ie, carcinoma in situ and gonadoblastoma). No VASA mRNA or protein was detectable in nonseminomatous germ cell tumors (such as embryonal carcinoma, teratoma, and yolk sac tumor) and derived cell lines, or nongerm cell tumors such as lymphoma or Leydig cell tumor. These results provide direct evidence that some germ cell tumors retain germ cell characteristics, whereas other tumors of germ cell origin result from differentiation and loss of germ cell identity. Furthermore, these findings suggest that VASA is likely to serve as a useful and highly specific biomarker for germ cell tumors, particularly classic and spermatocytic seminoma/dysgerminoma, including their precursor stages. (Lab Invest 2002, 82:159 -166).

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“…The first visual manifestation of dorsoventral polarity within the oocyte is the movement of the oocyte nucleus toward the dorsal side of the egg chamber, also via a microtubule-dependent mechanism (Koch andSpitzer 1983 GonzalezReyes et al 1995;Roth et al 1995). Subsequently, grk transcripts are localized tightly to the anterodorsal cortex of the oocyte, overlying the oocyte nucleus, in a process dependent on the function of the cappucino, spire, fs(1) KIO (KI 0), squid, and orb genes (Neuman-Silberberg and Schupbach 1993;Christerson and McKearin 1994). Reception of the Grk signal via the EGF receptor in the dorsal follicle cells is required for the synthesis of dorsal eggshell structures and the establishment of dorsoventral polarity in the embryo (Chasan and Anderson 1993; for review, see Schupbach and Roth 1994).…”

mentioning

confidence: 99%

Homeless is required for RNA localization in Drosophila oogenesis and encodes a new member of the DE-H family of RNA-dependent ATPases.

Gillespie¹,

Berg²

1995

Genes Dev.

155

151

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The homeless (hls) gene of Drosophila is required for anteroposterior and dorsoventral axis formation during oogenesis. At a low frequency, females homozygous for mutations in hls generate early egg chambers in which the oocyte is positioned incorrectly within the cyst. At a high frequency, late-stage egg chambers exhibit a ventralized chorion. Sequence analysis of the hls cDNA predicts a protein with amino-terminal homology to members of the DE-H family of RNA-dependent ATPases and putative helicases. Similarity of 51% in the amino-terminal third of the protein was found to two yeast splicing factors, PRP2 and PRP16, and to Drosophila Maleless, which is required for dosage compensation. To analyze Hls function, RNA localization patterns were determined for seven different transcripts in hls mutant ovaries. Previtellogenic transport to the oocyte was unaffected for all transcripts examined. Transport and localization of bicoid and oskm messages during vitellogenic stages were strongly disrupted, and the distribution and/or quantity of gurken, orb, and fs(3)KIO mRNAs were also affected, but to a lesser degree. In contrast, hu-li tai shao and Biicaudul-D transcripts were transported and localized normally in hls mutants. In addition, Kinesin heavy chain:p-Galactosidase fusion protein failed to localize correctly to the posterior of the oocyte in vitellogenic egg chambers. Examination of the microtubule structure with anti-a-Tubulin antibodies revealed aberrant microtubule organizing center movement and an abnormally dense cytoplasmic microtubule meshwork. We discuss potential roles for Hls in organizing a cytoskeletal framework essential for localizing specific RNAs.

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The drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGFα-like protein

Cited by 491 publications

References 62 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

VASA Is a Specific Marker for Both Normal and Malignant Human Germ Cells

Homeless is required for RNA localization in Drosophila oogenesis and encodes a new member of the DE-H family of RNA-dependent ATPases.

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