JNK functions in the non‐canonical Wnt pathway to regulate convergent extension movements in vertebrates

Yamanaka, Hiroaki; Moriguchi, Tetsuo; Masuyama, Norihisa; Kusakabe, Morioh; Hanafusa, Hiroshi; Takada, Ritsuko; Takada, Shinji; Nishida, Eisuke

doi:10.1093/embo-reports/kvf008

Cited by 403 publications

(370 citation statements)

References 26 publications

(41 reference statements)

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“…XRhoA Activates JNK in the Wnt/PCP Pathway During Xenopus CE Movements JNK is required for tissue polarity in flies and CE movements in frogs in the Wnt/PCP pathway (Strutt et al, 1997;Boutros et al, 1998;Paricio et al, 1999;Fanto et al, 2000;Weber et al, 2000;Yamanaka et al, 2002). Whereas Dsh regulates JNK activation through its DEP domain (Boutros et al, 1998;Li et al, 1999;Moriguchi et al, 1999;Habas et al, 2003), the involvement of Rho GTPases in JNK activation by Dsh remains unclear in mammalian cells (Li et al, 1999;Moriguchi et al, 1999;Habas et al, 2003).…”

Section: Resultsmentioning

confidence: 99%

“…However, the correlation between ROK␣ and JNK1 in the regulation of CE movements by RhoA remains unclear. JNK is involved in the nuclear response to PCP signaling in Drosophila (Mlodzik, 2002) and cell adhesion in Xenopus (Yamanaka et al, 2002). However, ROK regulates the cytoskeletal aspects in Drosophila and zebrafish (Mlodzik, 2002).…”

Section: Rok␣ Regulates Xenopus Ce Movements By Means Of Rhoa But Nomentioning

confidence: 99%

“…Furthermore, the specific domains of Dsh (Wharton, 2003) required for PCP signaling in CE movements during vertebrate gastrulation (Djiane et al, 2000;Heisenberg et al, 2000;Medina et al, 2000;Tada and Smith, 2000;Wallingford et al, 2000) are identical to those required in Drosophila (Axelrod et al, 1998;Boutros et al, 1998;Boutros and Mlodzik, 1999). In addition, CE movements in both Xenopus and zebrafish are controlled by the core PCP genes, including RhoA/Rac1 (Habas et al, 2001(Habas et al, , 2003Tahinci and Symes, 2003), JNK (Yamanaka et al, 2002), Rho-associated kinase-2 (ROK2, Marlow et al, 2002), Strabismus (Stbm, Darken et al, 2002;Goto and Keller, 2002;Jessen et al, 2002;Park and Moon, 2002), and Prickle (Takeuchi et al, 2003;Veeman et al, 2003a).…”

Section: Introductionmentioning

confidence: 99%

“…JNK is required for tissue polarity in flies and for CE movements in frogs (Boutros et al, 1998;Strutt et al, 1997;Paricio et al, 1999;Fanto et al, 2000;Weber et al, 2000;Yamanaka et al, 2002) and is regulated by several core PCP genes (Veeman et al, 2003b). In particular, Rho GTPases, including RhoA, Rac1, and Cdc42, play essential roles in JNK regulation.…”

Section: Introductionmentioning

confidence: 99%

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JNK and ROKα function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements

Kim

Han

2005

Developmental Dynamics

104

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The Wnt/planar cell polarity (PCP) pathway plays a critical role in wing, eye, and sensory bristle development of Drosophila and in convergent extension (CE) movements during vertebrate gastrulation. In Drosophila, Jun N-terminal kinase (JNK) and Rho-associated kinase (ROK) participate in RhoA-mediated PCP pathway during eye and wing development. In mammalian cells, Rac1 and Cdc42 but not RhoA are required for JNK activation by Wnt/PCP signals. However, there has been no evidence that Rho GTPases regulate JNK activation in Wnt/PCP pathway during Xenopus CE movements. Here, we report that Xenopus RhoA (XRhoA), but not Xenopus Cdc42 (XCdc42), is essential for JNK activation downstream of the Wnt/PCP pathway during Xenopus CE movements, and the phenotypic effect of loss of XRhoA function was rescued by Xenopus JNK1 (XeJNK1). In addition, XRhoA rescues the inhibition of CE movements by the DEP domain deletion mutant of Xenopus Dsh (Xdsh-⌬DEP), which has dominant negative (DN) effects on JNK activation, and the PDZ domain deletion mutant of Xdsh (Xdsh-⌬PDZ). Moreover, we demonstrate that Xenopus Rho-associated kinase ␣ (xROK␣), which is expressed mainly in mesoderm and ectoderm that undergo extensive cell rearrangements, regulates CE movements without affecting gene expression, and injection of xROK␣ rescued the inhibition of CE movements caused by DN XRhoA. Finally, we show that ROK␣ and JNK synergistically rescued embryos overexpressing DN XRhoA, which exhibit gastrulation defects, although ROK␣ is not required for JNK activation. Together, these data suggest that JNK and ROK␣ function in the noncanonical Wnt/RhoA pathway to regulate Xenopus CE movements. Developmental Dynamics 232: 958 -968, 2005.

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Section: Resultsmentioning

confidence: 99%

Section: Rok␣ Regulates Xenopus Ce Movements By Means Of Rhoa But Nomentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

JNK and ROKα function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements

Kim

Han

2005

Developmental Dynamics

104

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“…The migration of the cardiac neural crest is essential for parasympathetic innervation of the heart as well as completion of aortic-pulmonary septation (Kirby et al, 1983). Additionally, the JNK pathway has been implicated downstream of WNT signaling (Yamanaka et al, 2002), and WNT factors are critical to outflow tract formation. Knockout mice of Dishevelled 2, a modulator of the WNT pathway, exhibit neural tube defects as well as malformations of the cardiac outflow tract (Hamblet et al, 2002).…”

Section: Mekk4 (Omim#*602425)mentioning

confidence: 99%

MAP3Ks as central regulators of cell fate during development

Craig

Stevens

Vaillancourt

et al. 2008

Developmental Dynamics

108

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CK1ε and p120‐catenin control Ror2 function in noncanonical Wnt signaling

et al. 2018

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Canonical and noncanonical Wnt pathways share some common elements but differ in the responses they evoke. Similar to Wnt ligands acting through the canonical pathway, Wnts that activate the noncanonical signaling, such as Wnt5a, promote Disheveled (Dvl) phosphorylation and its binding to the Frizzled (Fz) Wnt receptor complex. The protein kinase CK1ε is required for Dvl/Fz association in both canonical and noncanonical signaling. Here we show that differently to its binding to canonical Wnt receptor complex, CK1ε does not require p120‐catenin for the association with the Wnt5a co‐receptor Ror2. Wnt5a promotes the formation of the Ror2–Fz complex and enables the activation of Ror2‐bound CK1ε by Fz‐associated protein phosphatase 2A. Moreover, CK1ε also regulates Ror2 protein levels; CK1ε association stabilizes Ror2, which undergoes lysosomal‐dependent degradation in the absence of this kinase. Although p120‐catenin is not required for CK1ε association with Ror2, it also participates in this signaling pathway as p120‐catenin binds and maintains Ror2 at the plasma membrane; in p120‐depleted cells, Ror2 is rapidly internalized through a clathrin‐dependent mechanism. Accordingly, downregulation of p120‐catenin or CK1ε affects late responses to Wnt5a that are also sensitive to Ror2, such as SIAH2 transcription, cell invasion, or cortical actin polarization. Our results explain how CK1ε is activated by noncanonical Wnt and identify p120‐catenin and CK1ε as two critical factors controlling Ror2 function.

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JNK functions in the non‐canonical Wnt pathway to regulate convergent extension movements in vertebrates

Cited by 403 publications

References 26 publications

JNK and ROKα function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements

JNK and ROKα function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements

MAP3Ks as central regulators of cell fate during development

CK1ε and p120‐catenin control Ror2 function in noncanonical Wnt signaling

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