hnRNP I is required to generate the Ca2+ signal that causes egg activation in zebrafish

Mei, Wenyan; Lee, Karen W.; Marlow, Florence; Miller, Andrew L.; Mullins, Mary C.

doi:10.1242/dev.037879

Cited by 56 publications

(62 citation statements)

References 65 publications

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“…We next labeled CGs in fixed eggs using fluorescent dye-conjugated Maclura pomifera agglutinin (MPA) (Becker and Hart, 1999;Dosch et al, 2004;Mei et al, 2009;Talevi et al, 1997). At 1 min post activation (mpa), CGE in WT and Mdchs1b eggs were comparable.…”

Section: Delayed Cge In Mdchs1b Mutantsmentioning

confidence: 99%

Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis

et al. 2015

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Dachsous (Dchs), an atypical cadherin, is an evolutionarily conserved regulator of planar cell polarity, tissue size, and cell adhesion. In humans, DCHS1 mutations cause pleiotropic Van Maldergem syndrome. Here, we report that mutations in zebrafish dchs1b and dchs2 disrupt several aspects of embryogenesis, including gastrulation. Unexpectedly, maternal zygotic (MZ) dchs1b mutants show defects in the earliest developmental stage, egg activation, including abnormal cortical granule exocytosis (CGE), cytoplasmic segregation, cleavages, and maternal mRNA translocation, in transcriptionally quiescent embryos. Later, MZdchs1b mutants exhibit altered dorsal organizer and mesendodermal gene expression, due to impaired dorsal determinant transport and Nodal signaling. Mechanistically, MZdchs1b phenotypes can be explained in part by defective actin or microtubule networks, which appear bundled in mutants. Accordingly, disruption of actin cytoskeleton in wild-type embryos phenocopied MZdchs1b mutant defects in cytoplasmic segregation and CGE. Whereas, interfering with microtubules in wild-type embryos impaired dorsal organizer and mesodermal gene expression without perceptible earlier phenotypes. Moreover, the bundled microtubule phenotype was partially rescued by expressing either full-length Dchs1b or its intracellular domain, suggesting Dchs1b affects microtubules and some developmental processes independent of its known ligand Fat. Our results indicate novel roles for vertebrate Dchs in actin and microtubule cytoskeleton regulation in the unanticipated context of the single-celled embryo.

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Section: Delayed Cge In Mdchs1b Mutantsmentioning

confidence: 99%

Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis

et al. 2015

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“…Cortical granules (CGs) are normally rapidly exocytosed following egg activation (Becker and Hart, 1999). Persisting CGs in zebrafish maternal-effect mutants disrupting heterogeneous nuclear ribonucleoprotein I (hnRNPI) are thought to interfere with vegetal pMTA formation and disrupt DV patterning (Mei et al, 2009). To determine whether persisting CGs could explain the disrupted pMTA in Mkif5Ba mutants, CGs were labeled with Maclura pomifera agglutinin (MPA) lectin Hart, 1996, 1999).…”

Section: Vegetal Microtubules Fail To Organize In Kif5ba Mutantsmentioning

confidence: 99%

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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“…The zebrafish egg cortex is composed of a meshwork of actin filaments (Hart and Collins, 1991;Becker and Hart, 1996). During oogenesis, membrane-bound cortical granules (CGs) accumulate throughout this egg cortex (Hart et al, 1987;Mei et al, 2009), and activation of the egg through water exposure triggers rapid granule exocytosis (Hart and Collins, 1991;Becker and Hart, 1999). Upon exocytosis, released CG products promote the lifting and hardening of the chorion (Wessel and Wong, 2009).…”

Section: Introductionmentioning

confidence: 99%

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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hnRNP I is required to generate the Ca2+ signal that causes egg activation in zebrafish

Cited by 56 publications

References 65 publications

Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis

Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis

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

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

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