Long Oskar Controls Mitochondrial Inheritance in Drosophila melanogaster

Hurd, Thomas R.; Herrmann, Beate; Sauerwald, Julia; Sanny, Justina; Grosch, Markus; Lehmann, Ruth

doi:10.1016/j.devcel.2016.11.004

Cited by 72 publications

(90 citation statements)

References 59 publications

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“…With no identifiable orthologs in humans, CG5726 protein shows up to 50% sequence identity among Drosophilids. In early embryos of Drosophila melanogaster, CG5726 interacts with short Osk (108). In this study, we found CG5726 to be interacting with multiple RBPs: Glo, Hrp48 and Vas, suggesting its possible role in translational regulation.…”

Section: Identification Of Novel Genes With a Potential Role In Drososupporting

confidence: 51%

“…Both SC35 and SF2 could be validated for their interaction with Glo and Stau, while pUF68 bound eIF4AIII and Stau in vitro. pUF68 was previously shown to interact with Hrp48 and Glo (38) and SF2 co-purifies with the short isoform of Osk (108). These results together with the well-studied role of SR proteins in cytoplasmic regulation of gene expression including mRNA export, decay and translation in mammalian systems (109,110) suggest that splicing factors are bona fide components of the mRNA localization machinery.…”

Section: Nuclear Processing Is Intrinsically Linked To Cytoplasmic Tamentioning

confidence: 65%

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An interaction network of RNA-binding proteins involved inDrosophilaoogenesis

Bansal

Madlung

Schaaf

et al. 2020

Preprint

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bioRxiv preprint Interactome of RNA Binding Proteins from Drosophila ovaries 2 Abbreviations used EGFP enhanced green fluorescent protein eIF eukaryotic initiation factor EJC exon junction complex FDR false discovery rate GO gene ontology HA Hemagglutinin hnRNP heterogeneous nuclear ribonucleoproteins IP immunoprecipitation LFQ label-free quantification MBP maltose-binding protein mRNP messenger ribonucleoprotein NMD nonsense-mediated decay PFA paraformaldehyde piRNA piwi-interacting RNA RBP RNA-binding proteins SILAC stable isotope labeling with amino acids UAS upstream activating sequence AbstractDuring Drosophila oogenesis, the localization and translational regulation of maternal transcripts relies on RNA-binding proteins (RBPs). Many of these RBPs localize several mRNAs and may have additional direct interaction partners to regulate their functions. Using immunoprecipitation from whole Drosophila ovaries coupled to mass spectrometry, we examined protein-protein associations of 6 GFP-tagged RBPs expressed at physiological levels. Analysis of the interaction network and further validation in human cells allowed us to identify 26 previously unknown associations, besides recovering several well characterized interactions. We identified interactions between RBPs and several splicing factors, providing links between nuclear and cytoplasmic events of mRNA regulation. Additionally, components of the translational and RNA decay machineries were selectively co-purified with some baits, suggesting a mechanism for how RBPs may regulate maternal transcripts. Given the evolutionary conservation of the studied RBPs, the interaction network presented here provides the foundation for future functional and structural studies of mRNA localization across metazoans. : bioRxiv preprint Interactome of RNA Binding Proteins from Drosophila ovaries 5 consistent with the role of their mammalian homologs (38, 50-52). During early oogenesis, both Vas and Nos are involved in the maintenance of germline stem cells, in oocyte differentiation and other aspects of oocyte development (26, 35, 53-56). In embryos, Nos functions in germline development (53, 57-61) and further promotes the inclusion of germline cells in the developing ovary (53, 62). In addition to oogenic processes, Nos and Stau are also involved in the development of the Drosophila nervous system (63, 64). Many RBPs in Drosophila oogenesis have overlapping functions that are likely differentially regulated. Little is known about this regulation and it may involve several as yet unidentified mRNP components. To comprehensively identify RBP interactors, we carried out a systematic in vivo purification screen of GFPtagged RBPs coupled with mass spectrometry. We employed both labeled and label-free MS methods and identified several proteins significantly enriched with the purified RBPs. The interactomes of the individual RBPs were largely independent with some overlap. Our screen identified several previously unknown interactions, many of which we validated in vitro. This work pres...

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Section: Identification Of Novel Genes With a Potential Role In Drososupporting

confidence: 51%

Section: Nuclear Processing Is Intrinsically Linked To Cytoplasmic Tamentioning

confidence: 65%

An interaction network of RNA-binding proteins involved inDrosophilaoogenesis

Bansal

Madlung

Schaaf

et al. 2020

Preprint

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“…This embryonic lethality was a strict maternal effect dependent on the temperature of the mother, which rescue experiments suggest is caused by incompatibility between the nuclear Aatm V and mitochondrial tRNA tyr G:U alleles. The temperature-shift experiments suggested that early oogenesis is a temperature-sensitive period, which is known to be a crucial time for mitochondrial proliferation, transport and selection, and alleles of mitochondrial proteins can even influence early oocyte specification (Cox and Spradling, 2003;Hill et al, 2014;Hurd et al, 2016;Ma et al, 2014;Teixeira et al, 2015). Our analysis, however, did not reveal defects in mitochondrial number, transport or oocyte specification.…”

Section: Discussioncontrasting

confidence: 57%

Incompatibility between mitochondrial and nuclear genomes during oogenesis results in ovarian failure and embryonic lethality

2017

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Mitochondrial dysfunction can cause female infertility. An important unresolved issue is the extent to which incompatibility between mitochondrial and nuclear genomes contributes to female infertility. It has previously been shown that a mitochondrial haplotype from D. simulans (simw 501) is incompatible with a nuclear genome from the D. melanogaster strain Oregon-R (OreR), resulting in impaired development, which was enhanced at higher temperature. This mitonuclear incompatibility is between alleles of the nuclear-encoded mitochondrial tyrosyl-tRNA synthetase (Aatm) and the mitochondrialencoded tyrosyl-tRNA that it aminoacylates. Here, we show that this mito-nuclear incompatibility causes a severe temperature-sensitive female infertility. The OreR nuclear genome contributed to death of ovarian germline stem cells and reduced egg production, which was further enhanced by the incompatibility with simw 501 mitochondria. Mito-nuclear incompatibility also resulted in aberrant egg morphology and a maternal-effect on embryonic chromosome segregation and survival, which was completely dependent on the temperature and mito-nuclear genotype of the mother. Our findings show that maternal mito-nuclear incompatibility during Drosophila oogenesis has severe consequences for egg production and embryonic survival, with important broader relevance to human female infertility and mitochondrial replacement therapy.

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“…In the Drosophila oocyte, streaming promotes the mixing and transport of cytoplasmic components (13,40) and is required for essential events for embryogenesis, such as the localization of mitochondria (41) and of the developmental determinant nanos mRNA (5,42).…”

Section: Discussionmentioning

confidence: 99%

Active diffusion and advection in theDrosophilaooplasm result from the interplay of the actin and microtubule cytoskeletons

Drechsler

Giavazzi

Cerbino

et al. 2017

Preprint

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Transport in cells occurs via a delicate interplay of passive and active processes, including diffusion, directed transport and advection. Despite progresses in super-resolution microscopy, discriminating and quantifying these processes is a challenge, requiring tracking of rapidly moving, sub-diffraction objects in a crowded, noisy environment. Here we use Differential Dynamic Microscopy with different contrast mechanisms to provide a thorough characterization of the dynamics in the Drosophila oocyte. We study the movement of vesicles and the elusive motion of a cytoplasmic F-actin mesh, a known regulator of cytoplasmic flows. We find that cytoplasmic motility constitutes a combination of directed motion and random diffusion. While advection is mainly attributed to microtubules, we find that active diffusion is driven by the actin cytoskeleton, although it is also enhanced by the flow. We also find that an important dynamic link exists between vesicles and cytoplasmic Factin motion, as recently suggested in mouse oocytes.

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Long Oskar Controls Mitochondrial Inheritance in Drosophila melanogaster

Cited by 72 publications

References 59 publications

An interaction network of RNA-binding proteins involved inDrosophilaoogenesis

An interaction network of RNA-binding proteins involved inDrosophilaoogenesis

Incompatibility between mitochondrial and nuclear genomes during oogenesis results in ovarian failure and embryonic lethality

Active diffusion and advection in theDrosophilaooplasm result from the interplay of the actin and microtubule cytoskeletons

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