Overexpression of oskar directs ectopic activation of nanos and presumptive pole cell formation in Drosophila embryos

Smith, Jeffrey L.; Wilson, Joan; Macdonald, Paul M.

doi:10.1016/0092-8674(92)90318-7

Cited by 193 publications

(157 citation statements)

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“…Among these, nanos (nos), germ cell-less (gcl), and polar granule component (pgc) have important roles in abdominal patterning and germ cell specification, germ cell formation, and germ cell transcriptional repression, respectively (18)(19)(20)(21)(22). All these functions fail in the absence of Osk and can be initiated at an ectopic location upon mislocalization of Osk (4,23).…”

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confidence: 99%

Structure of Drosophila Oskar reveals a novel RNA binding protein

Yang

et al. 2015

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

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Oskar (Osk) protein plays critical roles during Drosophila germ cell development, yet its functions in germ-line formation and body patterning remain poorly understood. This situation contrasts sharply with the vast knowledge about the function and mechanism of osk mRNA localization. Osk is predicted to have an N-terminal LOTUS domain (Osk-N), which has been suggested to bind RNA, and a C-terminal hydrolase-like domain (Osk-C) of unknown function. Here, we report the crystal structures of Osk-N and Osk-C. Osk-N shows a homodimer of winged-helix–fold modules, but without detectable RNA-binding activity. Osk-C has a lipase-fold structure but lacks critical catalytic residues at the putative active site. Surprisingly, we found that Osk-C binds the 3′UTRs of osk and nanos mRNA in vitro. Mutational studies identified a region of Osk-C important for mRNA binding. These results suggest possible functions of Osk in the regulation of stability, regulation of translation, and localization of relevant mRNAs through direct interaction with their 3′UTRs, and provide structural insights into a novel protein–RNA interaction motif involving a hydrolase-related domain.

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confidence: 99%

Structure of Drosophila Oskar reveals a novel RNA binding protein

Yang

et al. 2015

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

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“…Formation of the abdomen and pole cells requires localization of a large number of molecular determinants to the posterior pole of the developing oocyte (vasa protein, Hay et al 1988;Lasko and Ashburner 1990; oskar mRNA and protein, Ephrusso et al 1991;Kim-Ha et al 1991;Smith et al 1992; staufen protein, St. Johnston et al 1991; tudor protein, Bardsley et al 1993, nanos mRNA and protein, Wang and Lehmann 199 1 ; Ephrussi and Lehmann 1992j 'Corresponding author. Smith et al 1992; germ cell-less mRNA, Jongens et al 1994). The termini of the larva are marked during oogenesis by a signaling process between the oocyte and the surrounding epithelium of follicle cells (Stevens et al 1990; Savant-Bhonsale and Monte11 1993).…”

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confidence: 99%

“…The larval anterior is established during oogenesis through localization of the bicoid mRNA to the anterior end of the oocyte (Berleth et al 1988;Driever and Niisslein-Volhard 1988a,b). Formation of the abdomen and pole cells requires localization of a large number of molecular determinants to the posterior pole of the developing oocyte (vasa protein, Hay et al 1988;Lasko and Ashburner 1990;oskar mRNA and protein, Ephrusso et al 1991;Kim-Ha et al 1991;Smith et al 1992; staufen protein, St. Johnston et al 1991; tudor protein, Bardsley et al 1993, nanos mRNA and protein, Wang and Lehmann 199 1 ; Ephrussi and Lehmann 1992j 'Corresponding author.…”

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confidence: 99%

“…Johnston et al 1991; tudor protein, Bardsley et al 1993, nanos mRNA and protein, Wang and Lehmann 199 1 ; Ephrussi and Lehmann 1992j 'Corresponding author. Smith et al 1992; germ cell-less mRNA, Jongens et al 1994). The termini of the larva are marked during oogenesis by a signaling process between the oocyte and the surrounding epithelium of follicle cells (Stevens et al 1990;Savant-Bhonsale and Monte11 1993).…”

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confidence: 99%

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Cappuccino, a Drosophila maternal effect gene required for polarity of the egg and embryo, is related to the vertebrate limb deformity locus.

Emmons¹,

Phan²,

Calley³

et al. 1995

Genes Dev.

158

131

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ca puccino, a Droso hila maternal P ef ect gene required P or polarity of the egg and embryo, is related to the vertebrate limb deformity locus Steven Emmons, Huy Phan, John Calley, Wenliang Chen, Brian James, and Lynn ~anseau' Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona 85721 USA We report the molecular isolation of cappuccino (capu), a gene required for localization of molecular determinants within the developing Drosophila oocyte. The carboxy-terminal half of the capu protein is closely related to that of the vertebrate limb defo-ty locus, which is known to function in polarity determination in the developing vertebrate limb. In addition, capu shares both a proline-rich region and a 70-amino-acid domain with a number of other genes, two of which also function in pattern formation, the Saccharomyes cerevisiae BNIl gene and the Aspergillus FigA gene. We also show that capu mutant oocytes have abnormal microtubule distributions and premature microtubule-based cytoplasmic streaming within the oocyte, but that neither the speed nor the timing of the cytoplasmic streaming correlates with the strength of the mutant allele. This suggests that the premature cytoplasmic streaming in capu mutant oocytes does not suffice to explain the patterning defects. By inducing cytoplasmic streaming in wild-type oocytes during mid-oogenesis, we show that premature cytoplasmic streaming can displace staufen protein from the posterior pole, but not gurken mRNA from around the oocyte nucleus.[Key Words: Drosophila; cappuccino; pattern formation; cytoplasmic streaming; maternal effect; oogenesis; f ormins] Received July 5, 1995; revised version accepted August 25, 1995. The developing Drosophila oocyte is an excellent model system for studying the establishment of polarity within a single cell because the embryonic anterior-posterior and dorsal-ventral axes are initially organized within the oocyte. Anterior-posterior axis formation of the larva involves three pathways within the oocyte: one that establishes the anterior end, one at the posterior end to establish the abdomen and pole cells, and one at both termini of the oocyte to establish the ends (for reviews, see Manseau andSchupbach 1989a andNusslein-Volhard et al. 1987). The larval anterior is established during oogenesis through localization of the bicoid mRNA to the anterior end of the oocyte (Berleth et al. 1988; Driever and Niisslein-Volhard 1988a,b). Formation of the abdomen and pole cells requires localization of a large number of molecular determinants to the posterior pole of the developing oocyte (vasa protein, Hay et al. 1988;Lasko and Ashburner 1990; oskar mRNA and protein, Ephrusso et al. 1991;Kim-Ha et al. 1991;Smith et al. 1992; staufen protein, St. Johnston et al. 1991; tudor protein, Bardsley et al. 1993, nanos mRNA and protein, Wang and Lehmann 199 1 ; Ephrussi and Lehmann 1992j 'Corresponding author. Smith et al. 1992; germ cell-less mRNA, Jongens et al. 1994). The termini of the larva are marked during oogenesis b...

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“…In the case of germ plasm, the data to date suggest that this convergent phenotype results from distinct genetic pathways in different lineages. For example, the oskar gene has been shown to be sufficient for germ-plasm assembly in D. melanogaster (79)(80)(81). This gene has been identified in a number of insect lineages (66,82), but lacks known orthologs in noninsect metazoan lineages, including those with germ plasm (e.g., birds, fish, and frogs) (82).…”

Section: Is the Transition To Inheritance Mode Irreversible And Convementioning

confidence: 99%

Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans

Whittle

Extavour

2017

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

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In animals, primordial germ cells (PGCs) give rise to the germ lines, the cell lineages that produce sperm and eggs. PGCs form in embryogenesis, typically by one of two modes: a likely ancestral mode wherein germ cells are induced during embryogenesis by cell-cell signaling (induction) or a derived mechanism whereby germ cells are specified by using germ plasm-that is, maternally specified germ-line determinants (inheritance). The causes of the shift to germ plasm for PGC specification in some animal clades remain largely unknown, but its repeated convergent evolution raises the question of whether it may result from or confer an innate selective advantage. It has been hypothesized that the acquisition of germ plasm confers enhanced evolvability, resulting from the release of selective constraint on somatic gene networks in embryogenesis, thus leading to acceleration of an organism's protein-sequence evolution, particularly for genes expressed at early developmental stages, and resulting in high speciation rates in germ plasm-containing lineages (denoted herein as the "PGCspecification hypothesis"). Although that hypothesis, if supported, could have major implications for animal evolution, our recent large-scale coding-sequence analyses from vertebrates and invertebrates provided important examples of genera that do not support the hypothesis of liberated constraint under germ plasm. Here, we consider reasons why germ plasm might be neither a direct target of selection nor causally linked to accelerated animal evolution. We explore alternate scenarios that could explain the repeated evolution of germ plasm and propose potential consequences of the inheritance and induction modes to animal evolutionary biology.germ line | preformation | epigenesis | primordial germ cell | spandrel P rimordial germ cells (PGCs) are specialized cells located in sexual organs of animals. These cells are central to reproduction because they give rise to the germ lines and, ultimately, the sperm and eggs. The PGCs typically arise during early embryogenesis by one of two distinct modes: (i) induction, wherein germ cells are induced by cell-cell signaling pathways (also known as epigenesis); or (ii) inheritance, wherein germ cells are formed by using germ plasm (a specialized cytoplasm containing proteins and RNAs needed for PGC formation), that is, maternally generated germ-line determinants that are "preformed" before embryogenesis begins (also known as preformation) (1-3). The induction mode appears to be the more prevalent mode in animals and occurs in basally branching lineages, and thus is the hypothesized ancestral mechanism of PGC specification, whereas inheritance comprises the likely derived state (1) (Fig. 1) (see SI Appendix, section 1 on the less parsimonious scenario that induction is the derived mode). Induction has been inferred based on microscopic data from most animal clades studied to date and has been experimentally shown to occur in a diverse range of organisms, including mammals (Mus musculus) (4-8), salamanders (...

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Overexpression of oskar directs ectopic activation of nanos and presumptive pole cell formation in Drosophila embryos

Cited by 193 publications

References 43 publications

Structure of Drosophila Oskar reveals a novel RNA binding protein

Structure of Drosophila Oskar reveals a novel RNA binding protein

Cappuccino, a Drosophila maternal effect gene required for polarity of the egg and embryo, is related to the vertebrate limb deformity locus.

Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans

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