GBP binds kinesin light chain and translocates during cortical rotation in<i>Xenopus</i>eggs

Weaver, Carole; Farr, Gist H.; Pan, Weijun; Rowning, Brian A.; Wang, Jiyong; Mao, Junhao; Wu, Dianqing; Li, Lin; Larabell, Carolyn A.; Kimelman, David

doi:10.1242/dev.00737

Cited by 64 publications

(61 citation statements)

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“…5B). Several lines of evidence suggest that maternal determinants of the future dorsal axis in Xenopus embryos are composed of Wnt or subcellular components of the Wnt͞␤-catenin pathway, which inhibit the Axin͞ glycogen synthase kinase-3-mediated degradation of ␤-catenin in the cytoplasm (35,36). Although these maternal determinants are dorsally enriched in early Xenopus embryos, there are additional mechanisms to further confine the axis formation.…”

Section: Discussionmentioning

confidence: 99%

Jun NH ₂ -terminal kinase (JNK) prevents nuclear β-catenin accumulation and regulates axis formation in Xenopus embryos

Liao

Tao

Kofron

et al. 2006

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

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Jun NH2-terminal kinases (JNKs) regulate convergent extension movements in Xenopus embryos through the noncanonical Wnt͞ planar cell polarity pathway. In addition, there is a high level of maternal JNK activity spanning from oocyte maturation until the onset of gastrulation that has no defined functions. Here, we show that maternal JNK activation requires Dishevelled and JNK is enriched in the nucleus of Xenopus embryos. Although JNK activity is not required for the glycogen synthase kinase-3-mediated degradation of ␤-catenin, inhibition of the maternal JNK signaling by morpholino-antisense oligos causes hyperdorsalization of Xenopus embryos and ectopic expression of the Wnt͞␤-catenin target genes. These effects are associated with an increased level of nuclear and nonmembrane-bound ␤-catenin. Moreover, ventral injection of the constitutive-active Jnk mRNA blocks ␤-catenininduced axis duplication, and dorsal injection of active Jnk mRNA into Xenopus embryos decreases the dorsal marker gene expression. In mammalian cells, activation of JNK signaling reduces Wnt3A-induced and ␤-catenin-mediated gene expression. Furthermore, activation of JNK signaling rapidly induces the nuclear export of ␤-catenin. Taken together, these results suggest that JNK antagonizes the canonical Wnt pathway by regulating the nucleocytoplasmic transport of ␤-catenin rather than its cytoplasmic stability. Thus, the high level of sustained maternal JNK activity in early Xenopus embryos may provide a timing mechanism for controlling the dorsal axis formation. nucelocytoplasmic transport ͉ Wnt

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Section: Discussionmentioning

confidence: 99%

Jun NH ₂ -terminal kinase (JNK) prevents nuclear β-catenin accumulation and regulates axis formation in Xenopus embryos

Liao

Tao

Kofron

et al. 2006

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

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“…As predicted, inactivation of Wnt signaling results in ventralized embryos (for reviews, see Harland and Gerhart, 1997;Heasman, 1997;Sokol, 1999;Weaver and Kimelman, 2004;Schier and Talbot, 2005;Heasman, 2006;Tam et al, 2006;Rivera-Perez, 2007;White and Heasman, 2008;Langdon and Mullins, 2011;Houston, 2012). In Xenopus and zebrafish, the Wnt pathway is triggered by dorsal determinants localized to the vegetal pole of the egg (Fujisue et al, 1993;Holowacz and Elinson, 1995;Kikkawa et al, 1996;Kageura, 1997) and are probably positive components of the Wnt pathway (Larabell et al, 1996;Darras et al, 1997;Marikawa et al, 1997;Rowning et al, 1997;Marikawa and Elinson, 1999;Miller et al, 1999;Weaver et al, 2003;Tao et al, 2005;Cha et al, 2008). In response to sperm entry, these dorsal determinants are translocated from the vegetal pole to the future dorsal side of the embryo.…”

Section: Introductionmentioning

confidence: 89%

“…These disordered vegetal cortical microtubules soon become organized into numerous wavy parallel bundles (Elinson and Rowning, 1988;Houliston and Elinson, 1991b;Schroeder and Gard, 1992). Vesicle-like organelles, with which dorsal determinants are likely to be associated, are directionally transported along these microtubule arrays to the future dorsal side of the embryo Rowning et al, 1997;Miller et al, 1999;Weaver et al, 2003). In Xenopus embryos, vegetal cortical microtubules also serve as tracks to drive the rotation of the vegetal cortex (Houliston and Elinson, 1991a;Houliston, 1994;Houliston et al, 1994;Larabell et al, 1996).…”

Section: Introductionmentioning

confidence: 99%

Maternal Dead-End1 is required for vegetal cortical microtubule assembly during Xenopus axis specification

et al. 2013

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SUMMARYVertebrate axis specification is an evolutionarily conserved developmental process that relies on asymmetric activation of Wnt signaling and subsequent organizer formation on the future dorsal side of the embryo. Although roles of Wnt signaling during organizer formation have been studied extensively, it is unclear how the Wnt pathway is asymmetrically activated. In Xenopus and zebrafish, the Wnt pathway is triggered by dorsal determinants, which are translocated from the vegetal pole to the future dorsal side of the embryo shortly after fertilization. The transport of dorsal determinants requires a unique microtubule network formed in the vegetal cortex shortly after fertilization. However, molecular mechanisms governing the formation of vegetal cortical microtubule arrays are not fully understood. Here we report that Dead-End 1 (Dnd1), an RNA-binding protein required for primordial germ cell development during later stages of embryogenesis, is essential for Xenopus axis specification. We show that knockdown of maternal Dnd1 specifically interferes with the formation of vegetal cortical microtubules. This, in turn, impairs translocation of dorsal determinants, the initiation of Wnt signaling, organizer formation, and ultimately results in ventralized embryos. Furthermore, we found that Dnd1 binds to a uridine-rich sequence in the 3Ј-UTR of trim36, a vegetally localized maternal RNA essential for vegetal cortical microtubule assembly. Dnd1 anchors trim36 to the vegetal cortex in the egg, promoting high concentrations of Trim36 protein there. Our work thus demonstrates a novel and surprising function for Dnd1 during early development and provides an important link between Dnd1, mRNA localization, the microtubule cytoskeleton and axis specification.

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“…These include the Wnt ligands Wnt11 and Wnt5A (Tao et al, 2005;Cha et al, 2008), the receptors Frizzled7 (Sumanas et al, 2000) and Lrp6 (Kofron et al, 2007), and cytoplasmic proteins such as Disheveled (Dvl) (Sokol et al, 1995;Miller et al, 1999), Glycogen Synthase Kinase 3 (GSK3)-Binding Protein (GBP) (Yost et al, 1998;Dominguez and Green, 2000) and β-Catenin (Heasman et al, 1994. Interestingly, Green Fluorescent Protein (GFP)-tagged versions of both Dvl and GBP proteins were observed to translocate to the prospective dorsal side during cortical rotation, in association to vesicle-like organelles Miller et al, 1999;Weaver et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Maternal syntabulin is required for dorsal axis formation and is a germ plasm component in Xenopus

Colozza

Robertis

2014

Differentiation

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GBP binds kinesin light chain and translocates during cortical rotation inXenopuseggs

Cited by 64 publications

References 50 publications

Jun NH ₂ -terminal kinase (JNK) prevents nuclear β-catenin accumulation and regulates axis formation in Xenopus embryos

Jun NH ₂ -terminal kinase (JNK) prevents nuclear β-catenin accumulation and regulates axis formation in Xenopus embryos

Maternal Dead-End1 is required for vegetal cortical microtubule assembly during Xenopus axis specification

Maternal syntabulin is required for dorsal axis formation and is a germ plasm component in Xenopus

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GBP binds kinesin light chain and translocates during cortical rotation inXenopuseggs

Cited by 64 publications

References 50 publications

Jun NH 2 -terminal kinase (JNK) prevents nuclear β-catenin accumulation and regulates axis formation in Xenopus embryos

Jun NH 2 -terminal kinase (JNK) prevents nuclear β-catenin accumulation and regulates axis formation in Xenopus embryos

Maternal Dead-End1 is required for vegetal cortical microtubule assembly during Xenopus axis specification

Maternal syntabulin is required for dorsal axis formation and is a germ plasm component in Xenopus

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Jun NH ₂ -terminal kinase (JNK) prevents nuclear β-catenin accumulation and regulates axis formation in Xenopus embryos

Jun NH ₂ -terminal kinase (JNK) prevents nuclear β-catenin accumulation and regulates axis formation in Xenopus embryos