Looking at the Pretty “Phase” of Membraneless Organelles: A View From Drosophila Glia

Arkov, Alexey L.

doi:10.3389/fcell.2022.801953

Cited by 6 publications

(4 citation statements)

References 96 publications

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“…As Cup is removed from the mRNP complex, it may allow for another Bru1-binding factor to take its place, and stimulate translation of osk mRNA. This type of mRNA regulation is conserved beyond Drosophila oogenesis, such as in neuronal development, where both mRNA binding proteins and mRNAs stored in phase-separated condensates are necessary for proper memory formation (Tsang et al 2019) (reviewed in (Arkov 2022)). Here we show, for the first time, that a P-body component regulates the expression of an RNA-binding protein, suggesting that such a mechanism is broadly present in systems where spatio-temporal cues dictate mRNA translation.…”

Section: Discussionmentioning

confidence: 99%

Cup is essential foroskarmRNA translational repression during earlyDrosophilaoogenesis

Bayer

Milano

Formel

et al. 2023

Preprint

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The proper timing of mRNA translation is crucial across many biological systems for processes such as intercellular communication, body pattern formation, and morphogenesis. The main D. melanogaster posterior determinant, oskar, is maternally transcribed, but only translated when properly localized at the oocyte's posterior cortex. Bruno 1 and Cup are two effector proteins known to participate in multiple aspects of oskar mRNA regulation. Current model describes a mechanism in which Bruno 1 is necessary for Cup's recruitment to oskar mRNA, and Bruno 1 is indispensable for its translational repression. Here, we reveal that the Bruno 1-Cup interaction, as well as their interdependent influence on each other's mRNA and protein expression, lead to precise oskar mRNA regulation during early oogenesis. We show that these factors stably associate with the oskar mRNA in vivo, but surprisingly, Bruno 1's stable association with oskar mRNA depends on Cup, while Bruno 1 is not necessary for Cup association to oskar mRNA. During early oogenesis, Cup, not Bruno 1, is the essential factor for oskar mRNA repression. Cup is a crucial P-body member that maintains proper P-body morphology during oogenesis, as well as it is necessary for oskar mRNA's association with P-bodies, thus driving the translational repression and stability of oskar mRNA. Our experimental results collectively suggest a regulatory mechanism where a feedback loop between Bruno 1 and Cup coordinates oskar mRNA regulation in the egg chamber allowing for proper development to occur.

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Section: Discussionmentioning

confidence: 99%

Cup is essential foroskarmRNA translational repression during earlyDrosophilaoogenesis

Bayer

Milano

Formel

et al. 2023

Preprint

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“…Such mechanisms of mRNA regulation are conserved beyond Drosophila oogenesis, for example in neuronal development, where both mRNA binding proteins and mRNAs stored in phase-separated condensates are necessary for proper memory formation ([ 47 ], reviewed in [ 48 ]).…”

Section: Discussionmentioning

confidence: 99%

Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis

et al. 2023

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Study of the timing and location for mRNA translation across model systems has begun to shed light on molecular events fundamental to such processes as intercellular communication, morphogenesis, and body pattern formation. In D. melanogaster , the posterior mRNA determinant, oskar , is transcribed maternally but translated only when properly localized at the oocyte’s posterior cortex. Two effector proteins, Bruno1 and Cup, mediate steps of oskar mRNA regulation. The current model in the field identifies Bruno1 as necessary for Cup’s recruitment to oskar mRNA and indispensable for oskar ’s translational repression. We now report that this Bruno1-Cup interaction leads to precise oskar mRNA regulation during early oogenesis and, importantly, the two proteins mutually influence each other’s mRNA expression and protein distribution in the egg chamber. We show that these factors stably associate with oskar mRNA in vivo . Cup associates with oskar mRNA without Bruno1, while surprisingly Bruno1’s stable association with oskar mRNA depends on Cup. We demonstrate that the essential factor for oskar mRNA repression in early oogenesis is Cup, not Bruno1. Furthermore, we find that Cup is a key P-body component that maintains functional P-body morphology during oogenesis and is necessary for oskar mRNA’s association with P-bodies. Therefore, Cup drives the translational repression and stability of oskar mRNA. These experimental results point to a regulatory feedback loop between Bruno 1 and Cup in early oogenesis that appears crucial for oskar mRNA to reach the posterior pole and its expression in the egg chamber for accurate embryo development.

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“…Membraneless RNA-protein granules are assembled in all living systems and cell types and may represent one of the earliest levels of biological organization which has predated the cellular life 1 . Typically, the membraneless organelles are numerous and small structures (ranging from a few hundred nanometers to a few micrometers in diameter) and often their assembly process follows the principles of phase separation which occurs during formation of macromolecular condensates [2][3][4][5] .…”

Section: Introductionmentioning

confidence: 99%

Dynamic protein assembly and architecture of the large solitary membraneless organelle during germline development in the waspNasonia vitripennis

Kharel,

Tindell,

Kemph

et al. 2023

Preprint

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Germ cells in different animals assemble characteristic membraneless organelles referred to as germ granules, which contain RNA and proteins required for germline development. Typically, the germ granules are small spherical or amorphous cytoplasmic granules and often, they assemble around membrane-bound organelles such as nuclei, mitochondria and endoplasmic reticulum. In particular, in egg chambers of the fruit flyDrosophila, nurse cells assemble perinuclear granules, referred to as nuage, along with multiple small germ granules formed at the posterior pole of the oocyte (polar granules). Nuage is assembled in a very similar way in the waspNasonia vitripennis, despite the long evolutionary distance fromDrosophila.In contrast,Nasoniaforms a very different single germ granule, called the oosome, at the posterior, which is about 40 times larger than a homologousDrosophilapolar granule. Here, using molecular and super-resolution imaging approaches, we provide insights into protein assembly and architecture of the oosome during germline development. Interestingly, unlike the fly, the wasp utilizes alternatively spliced RNA-helicase Vasa isoforms during germline development and oosome formation. The isoforms differ by an unstructured region, containing repeats of phenylalanine and glycine, that is similar to functional domains characteristic of nucleoporins. In addition, while other conserved components of germ granules, such as Oskar, Aubergine and Tudor proteins are recruited to the oosome, these polypeptides show a distinct and specific localization within the oosome. Of particular note, Tudor protein forms a shell encapsulating the oosome, while small Oskar/Vasa/Aubergine granules occur inside the oosome core. Also, in surprising contrast toDrosophilaegg chambers, we found that a subset of the wasp nurse cells located in anterior show dramatic DNA damage and assemble higher levels of nuage than their posterior counterparts. The characteristics of two distinct nurse cell populations suggest a mechanistic link between the higher amounts of nuage assembled in anterior nurse cells and their need to silence transposable elements in the presence of double-strand DNA breaks. Our results point to the high degree of plasticity in the assembly of membraneless organelles, which adapt to specific developmental needs of different organisms, and suggest that novel molecular features of conserved proteins result in the unique architecture of the oosome in the wasp.

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Looking at the Pretty “Phase” of Membraneless Organelles: A View From Drosophila Glia

Cited by 6 publications

References 96 publications

Cup is essential foroskarmRNA translational repression during earlyDrosophilaoogenesis

Cup is essential foroskarmRNA translational repression during earlyDrosophilaoogenesis

Cup is essential for oskar mRNA translational repression during early Drosophila oogenesis

Dynamic protein assembly and architecture of the large solitary membraneless organelle during germline development in the waspNasonia vitripennis

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