Drosophila Rho-Associated Kinase (Drok) Links Frizzled-Mediated Planar Cell Polarity Signaling to the Actin Cytoskeleton

Winter, Christopher; Wang, Bruce; Ballew, Anna; Royou, Anne; Karess, Roger E.; Axelrod, Jeffrey; Luo, Liqun

doi:10.1016/s0092-8674(01)00298-7

Cited by 510 publications

(579 citation statements)

References 49 publications

(3 reference statements)

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“…Rho-GTPases have also been implicated in the morphogenesis of tissues in developing multicellular organisms. In Drosophila, the Rho-Rho-kinase pathway is involved in a number of morphogenetic-related PCP events, such as cellular rearrangement at germ band elongation and establishment of orientation of ommatidia and hairs (Winter et al, 2001;Bertet et al, 2004); and Rho, Rac, and Cdc42 regulate cytoskeletal reorganization of dorsal closure (Harden et al, 1999). In mice, the Rho-Rho-kinase pathway is involved in eyelid formation (Shimizu et al, 2005).…”

Section: Discussionmentioning

confidence: 99%

Apical Accumulation of Rho in the Neural Plate Is Important for Neural Plate Cell Shape Change and Neural Tube Formation

Kinoshita

Sasai

Misaki

et al. 2008

MBoC

102

118

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Although Rho-GTPases are well-known regulators of cytoskeletal reorganization, their in vivo distribution and physiological functions have remained elusive. In this study, we found marked apical accumulation of Rho in developing chick embryos undergoing folding of the neural plate during neural tube formation, with similar accumulation of activated myosin II. The timing of accumulation and biochemical activation of both Rho and myosin II was coincident with the dynamics of neural tube formation. Inhibition of Rho disrupted its apical accumulation and led to defects in neural tube formation, with abnormal morphology of the neural plate. Continuous activation of Rho also altered neural tube formation. These results indicate that correct spatiotemporal regulation of Rho is essential for neural tube morphogenesis. Furthermore, we found that a key morphogenetic signaling pathway, the Wnt/PCP pathway, was implicated in the apical accumulation of Rho and regulation of cell shape in the neural plate, suggesting that this signal may be the spatiotemporal regulator of Rho in neural tube formation.

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Section: Discussionmentioning

confidence: 99%

Apical Accumulation of Rho in the Neural Plate Is Important for Neural Plate Cell Shape Change and Neural Tube Formation

Kinoshita

Sasai

Misaki

et al. 2008

MBoC

102

118

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“…In Drosophila embryos, it also appears that Rok is the primary activating kinase of Sqh (myosin II regulatory light chain), and that Sqh is the primary target of Rok phosphorylation (Winter et al, 2001). Rok also phosphorylates and inactivates myosin light chain phosphatase, further promoting the phosphorylated and active state of Sqh (Mitonaka et al, 2007).…”

Section: Developmental Dynamicsmentioning

confidence: 99%

Assessing the critical period for Rho kinase activity during Drosophila ventral furrow formation

Krajcovic

Minden

2012

Developmental Dynamics

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Background: Drosophila ventral furrow formation (VFF), which is the first morphogenetic event during embryo development, serves as a model for epithelial sheet folding. VFF can be subdivided into five cell shape changes: apical membrane flattening, apicobasal nuclear migration, apicobasal cell shortening, random apical constriction, and concerted apical constriction. These processes are generally believed to be driven by Rho kinase (Rok) activation of myosin II to stimulate the constriction of the apical actomyosin network. To test the role of Rok and its downstream target myosin II in VFF, timed injections of the Rok inhibitor, Y-27632, were performed. Results: Embryos injected with Y-27632 before the concerted apical constriction phase of VFF were able to execute apicobasal nuclear migration and random apical constriction, but were unable to enter the concerted apical constriction phase. Embryos injected with Y-27632 during concerted apical constriction reverted to the transition point between random apical constriction and concerted apical constriction. Finally, embryos injected with Y-27632 upon the initiation of furrow ingression were able to complete VFF. Conclusions: Together these results suggest a critical period for Rok activity and presumably myosin II activation during the initiation of the concerted apical constriction phase of VFF.

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“…Rho-associated kinase (ROK) regulates cytoskeletal aspects of planar polarity in Drosophila (Winter et al, 2001) and CE movements in zebrafish . Xenopus ROK␣ (xROK␣) interacts with a Xenopus insulin receptor substrate-1 (xIRS-1) and acts as a potentiator of insulin-induced mitogen-activated protein kinase activation in Xenopus oocytes (Farah et al, 1998;Ohan et al, 1999).…”

Section: Rok␣ Is Involved In Xenopus Ce Movements Without Affecting Gmentioning

confidence: 99%

“…ROK regulates the cytoskeletal aspects of planar polarity in Drosophila (Winter et al, 2001) and CE movements in zebrafish . Data from the present study showed that xROK␣ regulates, as a target of XRhoA, CE movements in whole embryos and Keller explants without affecting gene expression.…”

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

confidence: 99%

“…Rho-associated kinase (ROK), a serine/threonine kinase effector of RhoA, plays essential roles in the cytoskeletal aspects of planar polarity in Drosophila through regulation of nonmuscle myosin II regulatory light chain phosphorylation and myosin II activity in PCP pathway (Winter et al, 2001). In zebrafish, ROK has been shown to regulate the cell polarity and motility by means of cell shape changes in CE movements .…”

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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Drosophila Rho-Associated Kinase (Drok) Links Frizzled-Mediated Planar Cell Polarity Signaling to the Actin Cytoskeleton

Cited by 510 publications

References 49 publications

Apical Accumulation of Rho in the Neural Plate Is Important for Neural Plate Cell Shape Change and Neural Tube Formation

Apical Accumulation of Rho in the Neural Plate Is Important for Neural Plate Cell Shape Change and Neural Tube Formation

Assessing the critical period for Rho kinase activity during Drosophila ventral furrow formation

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

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