Dynein light chain-dependent dimerization of Egalitarian is essential for maintaining oocyte fate in Drosophila

Neiswender, Hannah; Goldman, Chandler H.; Veeranan-Karmegam, Rajalakshmi; Gonsalvez, Graydon B.

doi:10.1016/j.ydbio.2021.06.009

Cited by 5 publications

(4 citation statements)

References 38 publications

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“…Egl has BicD-binding and Dynein light chain (Dlc)-binding domains at the oppositive ends of the protein and a central mRNA-binding domain (21, 26, 34). Dlc binding facilitates Egl dimerization and thus mRNA binding; in turn, Egl-mRNA binds BicD and gets attached to the dynein motor (32, 35, 67). We found that msps mRNA accumulation requires both dynein and the RNA binding Egl, suggesting that Egl links msps mRNA to dynein for dynein-dependent transport into the oocyte.…”

Section: Discussionmentioning

confidence: 99%

“…BicD is an adaptor that activates the motility of the dynein-dynactin complex and links the complex to its cargoes (29,30), whereas Egl, an RNA binding protein, serves as a key adaptor for dynein-dependent transport and is essential for the localization of the polarity determinants (e.g., oskar, gurken, and bicoid mRNAs) in oocytes and early embryos (31)(32)(33)(34)(35)(36). It raises a possibility that dynein transports some mRNA to the oocyte via its interaction with Egl, which in turn increases microtubule polymerization in the oocyte and promotes the oocyte fate determination and maintenance.…”

Section: Introductionmentioning

confidence: 99%

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Drosophilaoocyte specification is maintained by the dynamic duo of microtubule polymerase Mini spindles/XMAP215 and dynein

Lü

Lakonishok

Gelfand

2023

Preprint

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In many species, only one oocyte is specified among a group of interconnected germline sister cells. In Drosophila melanogaster, 16-cell interconnected cells form a germline cyst, where one cell differentiates into an oocyte, while the rest become nurse cells that supply the oocyte with mRNAs, proteins, and organelles through intercellular cytoplasmic bridges named ring canals via microtubule-based transport. In this study, we find that a microtubule polymerase Mini spindles (Msps), the Drosophila homolog of XMAP215, is essential for the oocyte fate determination. mRNA encoding Msps is concentrated in the oocyte by dynein-dependent transport along microtubules. Translated Msps stimulates microtubule polymerization in the oocyte, causing more microtubule plus ends to grow from the oocyte through the ring canals into nurse cells, further enhancing nurse cell-to-oocyte transport by dynein. Knockdown of msps blocks the oocyte growth and causes gradual loss of oocyte determinants. Thus, the Msps-dynein duo creates a positive feedback loop, enhancing dynein-dependent nurse cell-to-oocyte transport and transforming a small stochastic difference in microtubule polarity among sister cells into a clear oocyte fate determination.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Drosophilaoocyte specification is maintained by the dynamic duo of microtubule polymerase Mini spindles/XMAP215 and dynein

Lü

Lakonishok

Gelfand

2023

Preprint

View full text Add to dashboard Cite

show abstract

“…Egl has BicD-binding and Dlc-binding domains at the oppositive ends of the molecule and a central mRNA-binding domain ( 22 , 27 , 34 ). Dlc binding facilitates Egl dimerization and thus mRNA binding; in turn, Egl-mRNA binds BicD and gets attached to the dynein complex ( 32 , 35 , 68 ). We found that msps mRNA accumulation requires both dynein and the RNA-binding Egl, suggesting that Egl links msps mRNA to dynein for dynein-dependent transport into the oocyte.…”

Section: Discussionmentioning

confidence: 99%

“…The formation of MTOC is either blocked or disrupted in BicD and egl mutants ( 11 , 14 , 28 ). BicD is an adaptor that activates the motility of the dynein–dynactin complex and links the complex to its cargoes ( 29 , 30 ), whereas Egl, an RNA binding protein, serves as a key adaptor for dynein-dependent mRNA transport and is essential for the localization of the polarity determinants (e.g., oskar , gurken , and bicoid mRNAs) in oocytes and early embryos ( 31 – 36 ). However, the mechanism by which dynein regulates microtubule organization in the ovary through BicD and Egl remained elusive.…”

mentioning

confidence: 99%

The dynamic duo of microtubule polymerase Mini spindles/XMAP215 and cytoplasmic dynein is essential for maintaining Drosophila oocyte fate

Lu,

Lakonishok,

Gelfand

2023

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

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In many species, only one oocyte is specified among a group of interconnected germline sister cells. In Drosophila melanogaster , 16 interconnected cells form a germline cyst, where one cell differentiates into an oocyte, while the rest become nurse cells that supply the oocyte with mRNAs, proteins, and organelles through intercellular cytoplasmic bridges named ring canals via microtubule-based transport. In this study, we find that a microtubule polymerase Mini spindles (Msps), the Drosophila homolog of XMAP215, is essential for maintenance of the oocyte specification. mRNA encoding Msps is transported and concentrated in the oocyte by dynein-dependent transport along microtubules. Translated Msps stimulates microtubule polymerization in the oocyte, causing more microtubule plus ends to grow from the oocyte through the ring canals into nurse cells, further enhancing nurse cell-to-oocyte transport by dynein. Knockdown of msps blocks the oocyte growth and causes gradual loss of oocyte determinants. Thus, the Msps-dynein duo creates a positive feedback loop, ensuring oocyte fate maintenance by promoting high microtubule polymerization activity in the oocyte, and enhancing dynein-dependent nurse cell-to-oocyte transport.

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Bidirectional communication in oogenesis: a dynamic conversation in mice and Drosophila

Doherty

Amargant

Duncan

et al. 2022

Trends in Cell Biology

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Dynein light chain-dependent dimerization of Egalitarian is essential for maintaining oocyte fate in Drosophila

Cited by 5 publications

References 38 publications

Drosophilaoocyte specification is maintained by the dynamic duo of microtubule polymerase Mini spindles/XMAP215 and dynein

Drosophilaoocyte specification is maintained by the dynamic duo of microtubule polymerase Mini spindles/XMAP215 and dynein

The dynamic duo of microtubule polymerase Mini spindles/XMAP215 and cytoplasmic dynein is essential for maintaining Drosophila oocyte fate

Bidirectional communication in oogenesis: a dynamic conversation in mice and Drosophila

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