The Chromosomal Passenger Protein Birc5b Organizes Microfilaments and Germ Plasm in the Zebrafish Embryo

Nair, Sreelaja; Marlow, Florence; Abrams, Elliott W.; Kapp, Lee D.; Mullins, Mary C.; Pelegri, Francisco

doi:10.1371/journal.pgen.1003448

Cited by 44 publications

(131 citation statements)

References 57 publications

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“…7D,E,E′, arrows). These F-actin bands correspond to previously described circumferential F-actin arcs parallel to the outer rim of the blastodisc (Theusch et al, 2006;Nair et al, 2013b). At later stages (42-63 mpf ), which coincide with the period of cytokinesis for the first cell cycle, the circumferential F-actin bands persist and a contractile band develops at the site of furrow formation ( Fig.…”

Section: F-actin Reorganization Defects In Aura Mutantssupporting

confidence: 85%

aura/mid1ip1Lregulates the cytoskeleton at the zebrafish egg-to-embryo transition

2016

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Embryos from females homozygous for a recessive maternal-effect mutation in the gene aura exhibit defects including reduced cortical integrity, defective cortical granule (CG) release upon egg activation, failure to complete cytokinesis, and abnormal cell wound healing. Subcellular analysis shows that the cytokinesis defects observed in aura mutants are associated with aberrant cytoskeletal reorganization during furrow maturation, including abnormal F-actin enrichment and microtubule reorganization. Cortical F-actin prior to furrow formation fails to exhibit a normal transition into F-actin-rich arcs, and drug inhibition is consistent with aura function promoting F-actin polymerization and/or stabilization. In mutants, components of exocytic and endocytic vesicles, such as Vamp2, Clathrin and Dynamin, are sequestered in unreleased CGs, indicating a need for CG recycling in the normal redistribution of these factors. However, the exocytic targeting factor Rab11 is recruited to the furrow plane normally at the tip of bundling microtubules, suggesting an alternate anchoring mechanism independent of membrane recycling. A positional cloning approach indicates that the mutation in aura is associated with a truncation of Mid1 Interacting Protein 1L (Mid1ip1L), previously identified as an interactor of the X-linked Opitz G/BBB syndrome gene Mid1. A Cas9/CRISPR-induced mutant allele in mid1ip1L fails to complement the originally isolated aura maternal-effect mutation, confirming gene assignment. Mid1ip1L protein localizes to cortical F-actin aggregates, consistent with a direct role in cytoskeletal regulation. Our studies indicate that maternally provided aura/mid1ip1L acts during the reorganization of the cytoskeleton at the egg-to-embryo transition and highlight the importance of cytoskeletal dynamics and membrane recycling during this developmental period.

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Section: F-actin Reorganization Defects In Aura Mutantssupporting

confidence: 85%

aura/mid1ip1Lregulates the cytoskeleton at the zebrafish egg-to-embryo transition

2016

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“…To date, zebrafish mutants disrupting GP assembly during early cleavages also perturb cleavages (Nair et al, 2013;Pelegri et al, 1999;Yabe et al, 2009). Both microtubule (MT) and F-actin networks are implicated in GP accumulation at cleavage furrows (Nair et al, 2013;Pelegri et al, 1999;Theusch et al, 2006;Yabe et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…Both microtubule (MT) and F-actin networks are implicated in GP accumulation at cleavage furrows (Nair et al, 2013;Pelegri et al, 1999;Theusch et al, 2006;Yabe et al, 2009). MTs are enriched in distal cleavage furrows (Jesuthasan, 1998), and MT tips colocalize with GP-RNPs (Nair et al, 2013); however, it is unknown whether specific aggregation or stabilization factors exist and whether molecular motors are involved. Buc, a female germline-specific protein, is necessary and sufficient for Bb formation, in which GP localizes in primary oocytes (Bontems et al, 2009;Heim et al, 2014;Marlow and Mullins, 2008), and zebrafish and Xenopus Buc/Velo interact with RNAbps that bind GP-RNAs (Heim et al, 2014;Nijjar and Woodland, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Kinesin-1 interacts with Bucky ball to form germ cells and is required to pattern the zebrafish body axis

et al. 2015

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In animals, specification of the primordial germ cells (PGCs), the stem cells of the germline, is required to transmit genetic information from one generation to the next. Bucky ball (Buc) is essential for germ plasm (GP) assembly in oocytes and its overexpression results in excess PGCs in zebrafish embryos. However, the mechanistic basis for the excess PGCs in response to Buc overexpression, and whether endogenous Buc functions during embryogenesis are unknown. Here we show that endogenous Buc, like GP and overexpressed Buc-GFP, accumulates at embryonic cleavage furrows. Furthermore, we show that the maternally expressed zebrafish Kinesin-1 Kif5Ba is a binding partner of Buc and that maternal kif5Ba (Mkif5Ba) plays an essential role in germline specification in vivo. Specifically, Mkif5Ba is required to recruit GP to cleavage furrows and thereby specifies PGCs. Moreover, Mkif5Ba is required to enrich Buc at cleavage furrows and for Buc’s ability to promote excess PGCs, providing mechanistic insight into how Buc functions to assemble embryonic GP. In addition, we show that Mkif5Ba is also essential for dorsoventral (DV) patterning. Specifically, Mkif5Ba promotes formation of the parallel vegetal microtubule array required to asymmetrically position dorsal determinants (DDs) towards the prospective dorsal side. Interestingly, while Syntabulin and wnt8a translocation depend on kif5Ba, grip2a translocation does not, providing evidence for two distinct mechanisms by which DDs may be asymmetrically distributed. These studies identify essential roles for maternal Kif5Ba in PGC specification and DV patterning and provide mechanistic insight into Buc functions during early embryogenesis.

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“…1A–E and Kimmel et al, 1995). Mature eggs are arrested at metaphase of meiosis II, which progresses and completes with the extrusion of the second polar body within minutes of the egg coming into contact with water (Selman et al, 1993; Dekens et al, 2003; Nair et al, 2013). If fertilization occurs, egg activation and the initial steps of pronuclear congression and fusion occur concurrently, followed by iterative zygotic mitoses.…”

Section: Resultsmentioning

confidence: 99%

Transient window of resilience during early development minimizes teratogenic effects of heat in zebrafish embryos

Menon

Nair

2018

Developmental Dynamics

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Background: Transient heat shock during early development is an established experimental paradigm for doubling the genome of the zebrafish zygote, which has practical applications in expedited identification of recessive mutations in genetic screens. Despite the simplicity of the strategy and the genetic tractability of zebrafish, heat shock has not been used for genome doubling since the proof‐of‐principle experiments done in the 1980s. This is because of poor survival of embryos that ensue from transient heat shocks and gross developmental abnormalities in the few survivors, which is incompatible with phenotype driven screens. Results: We show that heat shocks during early zebrafish development uncouple the second cycle of DNA and centrosome duplication. Interestingly, the developmental time of the heat shock that triggers the dissociation between DNA and centrosome duplication cycles significantly affect the potential of embryos to survive and attain normal morphology. The potential to develop normally after a heat shock alters in a developmental time span of 2 min in zebrafish embryos, a phenomenon that has not been reported in any species. Conclusions: The existence of heat resilient developmental windows and reduced heat teratogenicity during these windows could be an effective step forward in practical application of transient heat for experimental manipulation of ploidy in zebrafish. More broadly, heat resilience before zygotic genome activation suggests that metazoan embryos may possess innate protective features against heat beyond the canonical heat shock response. Developmental Dynamics 247:992–1004, 2018. © 2018 Wiley Periodicals, Inc.

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The Chromosomal Passenger Protein Birc5b Organizes Microfilaments and Germ Plasm in the Zebrafish Embryo

Cited by 44 publications

References 57 publications

aura/mid1ip1Lregulates the cytoskeleton at the zebrafish egg-to-embryo transition

aura/mid1ip1Lregulates the cytoskeleton at the zebrafish egg-to-embryo transition

Kinesin-1 interacts with Bucky ball to form germ cells and is required to pattern the zebrafish body axis

Transient window of resilience during early development minimizes teratogenic effects of heat in zebrafish embryos

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