Novel role of specific Tudor domains in Tudor–Aubergine protein complex assembly and distribution during Drosophila oogenesis

Creed, T. Michael; Loganathan, Sudan N.; Varonin, Dan; Jackson, Christina A.; Arkov, Alexey L.

doi:10.1016/j.bbrc.2010.10.040

Cited by 13 publications

(10 citation statements)

References 28 publications

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“…To determine the detailed distribution of integral interacting polar granule proteins, Tud and Aub, we carried out super-resolution confocal imaging of the granules immunostained with anti-GFP antibody (to label functional GFP-tagged Tud that we previously described 20 ) and specific anti-Aub antibody 21 . GFP-Tud shows the localization to germ plasm and germ cells 20,22 as the untagged Tud 23 , indicating that GFP-Tud is a reliable marker of polar granules.…”

Section: Resultsmentioning

confidence: 99%

Protein components of ribonucleoprotein granules from Drosophila germ cells oligomerize and show distinct spatial organization during germline development

Wahiduzzaman

Tindell

et al. 2019

Sci Rep

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The assembly of large RNA-protein granules occurs in germ cells of many animals and these germ granules have provided a paradigm to study structure-functional aspects of similar structures in different cells. Germ granules in Drosophila oocyte’s posterior pole (polar granules) are composed of RNA, in the form of homotypic clusters, and proteins required for germline development. In the granules, Piwi protein Aubergine binds to a scaffold protein Tudor, which contains 11 Tudor domains. Using a super-resolution microscopy, we show that surprisingly, Aubergine and Tudor form distinct clusters within the same polar granules in early Drosophila embryos. These clusters partially overlap and, after germ cells form, they transition into spherical granules with the structural organization unexpected from these interacting proteins: Aubergine shell around the Tudor core. Consistent with the formation of distinct clusters, we show that Aubergine forms homo-oligomers and using all purified Tudor domains, we demonstrate that multiple domains, distributed along the entire Tudor structure, interact with Aubergine. Our data suggest that in polar granules, Aubergine and Tudor are assembled into distinct phases, partially mixed at their “interaction hubs”, and that association of distinct protein clusters may be an evolutionarily conserved mechanism for the assembly of germ granules.

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Section: Resultsmentioning

confidence: 99%

Protein components of ribonucleoprotein granules from Drosophila germ cells oligomerize and show distinct spatial organization during germline development

Wahiduzzaman

Tindell

et al. 2019

Sci Rep

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“…Immunohistochemistry. Drosophila ovary immunostaining was performed as previously described 14,51,52 .…”

Section: Drosophila Embryo Chemical Crosslinking and Me31b Complex Pumentioning

confidence: 99%

Comparative Proteomics Reveal Me31B’s Interactome Dynamics, Expression Regulation, and Assembly Mechanism into Germ Granules during Drosophila Germline Development

McCambridge

Solanki

Olchawa

et al. 2020

Sci Rep

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Me31B is a protein component of Drosophila germ granules and plays an important role in germline development by interacting with other proteins and RNAs. To understand the dynamic changes that the Me31B interactome undergoes from oogenesis to early embryogenesis, we characterized the early embryo Me31B interactome and compared it to the known ovary interactome. The two interactomes shared RNA regulation proteins, glycolytic enzymes, and cytoskeleton/motor proteins, but the core germ plasm proteins Vas, Tud, and Aub were significantly decreased in the embryo interactome. Our follow-up on two RNA regulations proteins present in both interactomes, Tral and Cup, revealed that they colocalize with Me31B in nuage granules, P-bodies/sponge bodies, and possibly in germ plasm granules. We further show that Tral and Cup are both needed for maintaining Me31B protein level and mRNA stability, with Tral's effect being more specific. In addition, we provide evidence that Me31B likely colocalizes and interacts with germ plasm marker Vas in the ovaries and early embryo germ granules. Finally, we show that Me31B's localization in germ plasm is likely independent of the Osk-Vas-Tud-Aub germ plasm assembly pathway although its proper enrichment in the germ plasm may still rely on certain conserved germ plasm proteins. Germ cells are essential for sexual reproduction and the survival of many species, and species-specific strategies exist to form germ cells 1-5. Drosophila melanogaster uses maternally inherited germ granules to determine germ cell fate. Germ granules are heterogeneous aggregates of ribonucleoprotein (RNP) complexes 6 that undergo dynamic positional, morphological, and compositional changes during germline development, a process that spans oogenesis and early embryogenesis 7-11. Me31B, a conserved germ granule component 9,12 , is expressed in nurse cells, oocytes, and early embryos 13. In these cells, Me31B exists in different types of RNP granules, including nuage granules, P-bodies, sponge bodies, and germ plasm granules 12-15. In these granules, Me31B has been suggested to function as a putative ATP-dependent RNA helicase that interacts with other germline proteins and RNAs to exert post-transcriptional regulation on those RNAs 10,11,13,16,17. As an important example, Me31B associates with osk mRNA to ensure its proper translation into Osk protein only at the posterior pole of developing oocytes. Then, the Osk protein initiates a step-wise assembly pathway that recruits downstream proteins including Vas, Tud, and Aub to form the germ plasm and eventually dictates germ cell formation 13,18-21. Me31B exhibits changes in its localization pattern, aggregation status, and even function as germline cells develop during the ovary-to-embryo transition 13,17. It is believed that these changes are correlated with the different biological contexts in which Me31B exists 17. Therefore, to understand the role of Me31B during germ

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“…The germline gene Tudor contains 11 Tudor-domain repeats and is required for polar granule formation (8, 91, 115). Aub and Ago3 bind to Tudor in a sDMA-dependent manner and this binding is required for germ plasm assembly and PGC specification (24, 50, 51, 82) (Table 2). In Drosophila , PRMT5 is required for arginine methylation of Piwi proteins (50, 72).…”

Section: The Expression and Function Of Piwi Proteins In The Germlinementioning

confidence: 99%

Uniting Germline and Stem Cells: The Function of Piwi Proteins and the piRNA Pathway in Diverse Organisms

2011

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The topipotency of the germline is the full manifestation of the pluri- and multipotency of embryonic and adult stem cells, thus the germline and stem cells must share common mechanisms that guarantee their multipotentials in development. One of the few such known shared mechanisms is represented by Piwi proteins, which constitute one of the two subfamilies of the Argonaute protein family. Piwi proteins bind to Piwi-interacting RNAs (piRNAs) that are generally 26–31 nucleotides in length. Both Piwi proteins and piRNAs are most abundantly expressed in the germline. Moreover, Piwi proteins are expressed broadly in certain types of somatic stem/progenitor cells and other somatic cells across animal phylogeny. Recent studies indicate that the Piwi-piRNA pathway mediates epigenetic programming and post-transcriptional regulation, which may be responsible for its function in germline specification, gametogenesis, stem cell maintenance, transposon silencing, and genome integrity in diverse organisms.

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Novel role of specific Tudor domains in Tudor–Aubergine protein complex assembly and distribution during Drosophila oogenesis

Cited by 13 publications

References 28 publications

Protein components of ribonucleoprotein granules from Drosophila germ cells oligomerize and show distinct spatial organization during germline development

Protein components of ribonucleoprotein granules from Drosophila germ cells oligomerize and show distinct spatial organization during germline development

Comparative Proteomics Reveal Me31B’s Interactome Dynamics, Expression Regulation, and Assembly Mechanism into Germ Granules during Drosophila Germline Development

Uniting Germline and Stem Cells: The Function of Piwi Proteins and the piRNA Pathway in Diverse Organisms

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