Bucky Ball Is a Novel Zebrafish Vasa ATPase Activator

Perera, Roshan Priyarangana; Shaikhqasem, Alaa; Rostam, Nadia; Dickmanns, Achim; Tittmann, Kai; Dosch, Roland

doi:10.3390/biom11101507

Cited by 4 publications

(4 citation statements)

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“…The report of Perera et al further specified the vasa-binding motif in zebrafish (Fig. 1 in 18 ) to a shorter 23 amino acid sequence. Remarkably, this short motif matches 75% of chicken Bucky ball amino acid sequence (Fig.…”

Section: Discussionmentioning

confidence: 96%

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Identification of chicken LOC420478 as Bucky ball equivalent and potential germ plasm organizer in birds

Klein

Dosch

Altgilbers

et al. 2022

Sci Rep

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Bucky ball was identified as germ plasm organizer in zebrafish and has proven crucial for Balbiani body condensation. A synteny comparison identified an uncharacterized gene locus in the chicken genome as predicted avian counterpart. Here, we present experimental evidence that this gene locus indeed encodes a ‘Bucky ball’ equivalent in matured oocytes and early embryos of chicken. Heterologous expression of Bucky ball fusion proteins both from zebrafish and chicken with a fluorescent reporter revealed unique patterns indicative for liquid–liquid phase separation of intrinsically disordered proteins. Immuno-labeling detected Bucky ball from oocytes to blastoderms with diffuse distribution in matured oocytes, aggregation in first cleavage furrows, and co-localization to the chicken vasa homolog (CVH). Later, Bucky ball translocated to the cytoplasm of first established cells, and showed nuclear translocation during the major zygotic activation together with CVH. Remarkably, during the phase of area pellucida formation, Bucky ball translocated back into the cytoplasm at stage EGK VI, whereas CVH remained within the nuclei. The condensation of Bucky ball and co-localization with CVH in cleavage furrows and nuclei of the centrally located cells strongly suggests chicken Bucky ball as a germ plasm organizer in birds, and indicate a special importance of the major zygotic activation for germline specification.

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Section: Discussionmentioning

confidence: 96%

“…For the separation of the germ plasm from the rest of cytoplasm, the IDP Bucky ball provides essential liquid–liquid phase separation properties 11 , 17 . In zebrafish mutants lacking a short, 23 amino acid sequence of Bucky ball, localized Vasa activation is not observed and germ cell specification is disrupted 12 , 18 .…”

Section: Introductionmentioning

confidence: 99%

Identification of chicken LOC420478 as Bucky ball equivalent and potential germ plasm organizer in birds

Klein

Dosch

Altgilbers

et al. 2022

Sci Rep

Self Cite

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“…The copyright holder for this preprint (which this version posted July 19, 2023. ; https://doi.org/10.1101/2023.07.18.549483 doi: bioRxiv preprint localizes to both germ granules in PGCs [3,57,58] and Bb granules [13,57] and is essential for both [20,57,59]. Tdrd6a localizes to all three granule types [51], is essential for PGCs, dispensable in the piRNA pathway, and modifies Buc aggregation and Bb morphology [51].…”

Section: Discussionmentioning

confidence: 99%

“…First, RNP granules that contain germ cell fate determinants, termed germ plasm, initially specify PGCs in the embryo, and then maintain their germ fate and are required for their proper migration to the gonad [1]. The germ plasm includes the RNP components Vasa, Dead-end (Dnd), and Bucky ball (Buc) [2,3].A second type of RNP granules is called germ granules and form in oogonia and early differentiating oocytes in the ovary [4]. Germ granules are localized perinuclearly and contain the PIWI interacting RNAs (piRNA) pathway machinery [5], which protects germline nuclei from retrotransposons by processing and cleaving their transcripts [4][5][6][7][8].…”

Section: Introductionmentioning

confidence: 99%

The piRNA protein Asz1 is essential for germ cell and gonad development in zebrafish and exhibits differential necessities in distinct types of RNP granules

Ahmad,

Bogoch,

Shvaizer

et al. 2023

Preprint

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Germ cells are essential for fertility, embryogenesis, and reproduction. Germline development requires distinct types of RNA-protein (RNP) granules, including germ plasm in embryos, piRNA granules in gonadal germ cells, and the Balbiani body (Bb) in oocytes. However, the regulation of RNP assemblies in zebrafish germline development are still poorly understood. Asz1 is a piRNA protein in Drosophila and mice. Zebrafish Asz1 localizes to both piRNA and Bb granules, with yet unknown functions. Here, we hypothesized that Asz1 functions in RNP granule assemblies and germline development in zebrafish. We generated asz1 mutant fish to determine the roles of Asz1 in germ cell development. We show that Asz1 is dispensable for somatic development, but essential for germ cell and gonad development. asz1-/- fish developed exclusively as sterile males with severely underdeveloped testes that lacked germ cells, demonstrating that Asz1 is essential for spermatogenesis. Mechanistically, we provide evidence to conclude that zygotic Asz1 is not required for primordial germ cell specification or migration to the gonad, but is essential for germ cell survival during post-embryonic gonad development, likely by suppressing the expression of germline transposons. Increased transposon expression and morphologically mis-organized piRNA granules in asz1 mutants, argues that zebrafish Asz1 functions in the piRNA pathway. We generated asz1;tp53 fish to partially rescue ovarian development, revealing underdeveloped mutant ovaries with defective oocytes, and that Asz1 is also essential for oogenesis. We further showed that in contrast with piRNA granules, Asz1 is dispensable for Bb granule formation, as shown by normal Bb localization of Buc and dazl. By uncovering Asz1 as an essential regulator of germ cell survival and gonadogenesis in zebrafish, and determining its differential necessity in distinct RNP granule types, our work advances our understanding of the developmental genetics of reproduction and fertility, as well as of RNP granule biology.

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Interplay of RNA-binding proteins controls germ cell development in zebrafish

Shi

2024

Journal of Genetics and Genomics

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Bucky Ball Is a Novel Zebrafish Vasa ATPase Activator

Cited by 4 publications

References 50 publications

Identification of chicken LOC420478 as Bucky ball equivalent and potential germ plasm organizer in birds

Identification of chicken LOC420478 as Bucky ball equivalent and potential germ plasm organizer in birds

The piRNA protein Asz1 is essential for germ cell and gonad development in zebrafish and exhibits differential necessities in distinct types of RNP granules

Interplay of RNA-binding proteins controls germ cell development in zebrafish

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