Stat3 Controls Cell Movements during Zebrafish Gastrulation

Yamashita, Susumu; Miyagi, Chiemi; Carmany-Rampey, Amanda; Shimizu, Takashi; Fujii, Ritsuko; Schier, Alexander F.; Hirano, Toshio

doi:10.1016/s1534-5807(02)00126-0

Cited by 171 publications

(153 citation statements)

References 60 publications

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“…Our recent results show that zebrafish dpr2 functions in regulation of convergence and extension movements during gastrulation (Waxman et al, 2004). Research by Yamashita et al (2002) showed that ␤-catenin signaling somehow increased phosphorylation of Stat3, which regulates proper convergence and extension movements. Thus, ␤-catenin activation of dpr2 constitutes the second known example of ␤-catenin signaling regulating morphogenesis and the first in which regulation is at the level of transcription.…”

Section: Positive Feedback Loops and Cross-regulation Of Signaling Pamentioning

confidence: 77%

“…The accumulation of ␤-catenin on the future dorsal side leads to the expression of genes of the dorsal organizer and, in at least one case, potentiation of the action of an organizer protein (Kelly et al, 2000;Ryu et al, 2001;Solnica-Krezel and Driever, 2001;Yamashita et al, 2002;Dougan et al, 2003). Organizer genes promote dorsal axis formation in three important ways: by antagonizing the activity of ventralizing genes, by establishing dorsal mesendoderm, and by promoting proper gastrulation movements.…”

Section: Introductionmentioning

confidence: 99%

“…Members of the Nodal family, squint (sqt) and cyclops (cyc), are also either direct or indirect targets of ␤-catenin and are responsible for specifying dorsal mesendoderm (Schier et al, 1997;Dougan et al, 2003). Finally, ␤-catenin promotes phosphorylation of Stat3 leading to proper convergence and extension movements (Yamashita et al, 2002). Thus, ␤-catenin plays multiple roles in dorsal axis specification.…”

Section: Introductionmentioning

confidence: 99%

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Regulation of the early expression patterns of the zebrafish Dishevelled-interacting proteins Dapper1 and Dapper2

Waxman

2005

Dev. Dyn.

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The Dapper/Frodo family of proteins are Dishevelled-interacting regulators of Wnt signaling. In this study, I characterize the regulation of the early expression patterns of dpr1 and dpr2. Although both dpr1 and dpr2 are expressed on the prospective dorsal side, I find that their pregastrula expression patterns have differences that have not been reported previously. Early dpr1 expression is much more dynamic than dpr2 expression. I use gain and loss of function experiments to identify dorsal organizer genes that regulate dpr1 and dpr2 expression. The dorsalizing factors ␤-catenin, Bozozok (Boz), Noggin (Nog), and the mesendoderminducing factor Squint (Sqt) are all able to induce ectopic expression of dpr1 and dpr2. In reciprocal loss of function experiments, loss of maternal ␤-catenin signaling leads to loss of early dorsal dpr1 and dpr2 expression, whereas loss of Boz and/or Nodal signaling does not. Ectopic expression of the ventralizing molecule Bmp2b leads to reduction of dpr1 and dpr2 expression. These results suggest that, in early zebrafish development, dpr1 and dpr2 are targets of ␤-catenin and/or an unknown downstream effector.

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Section: Positive Feedback Loops and Cross-regulation Of Signaling Pamentioning

confidence: 77%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Regulation of the early expression patterns of the zebrafish Dishevelled-interacting proteins Dapper1 and Dapper2

Waxman

2005

Dev. Dyn.

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“…STAT3 has been shown to be required for cell motility in a few other contexts. Essential role of STAT3 was shown in epithelial to mesenchymal transition during zebrafish embryo gastrulation (Yamashita et al, 2002). STAT3-deficient keratinocytes showed increased cell adhesiveness and compromised growth factor-inducible cell migration, accompanying with an increased hyperphosphorylation of focal adhesion and its component protein p130cas (Kira et al, 2002).…”

Section: Discussionmentioning

confidence: 99%

Requirement of STAT3 activation for maximal collagenase-1 (MMP-1) induction by epidermal growth factor and malignant characteristics in T24 bladder cancer cells

et al. 2005

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Signal transducers and activators of transcription (STATs) are latent transcription factors that mediate cytokine-and growth factor-induced transcription. Constitutive activation of STAT3 has been shown in human cancers and transformed cell lines. We report that STAT3, but not STAT1 and STAT5, becomes phosphorylated in response to epidermal growth factor (EGF) and achieves maximal induction of collagenase-1 (MMP-1) transcription by interacting with c-JUN. Phosphorylation of STAT3 protein is biphasic: the first peak within 30 min and the second peak between 4 and 8 h. Association of STAT3 with c-JUN is detected and its constituting STAT3 is increasingly phosphorylated. The STAT and AP-1 elements are necessary for effective induction of MMP-1 promoter by EGF. Mutation of AP-1 element closely located at the STAT site abolishes the binding not only of c-JUN but also of STAT3 to MMP-1 promoter, resulting in the loss of the responsiveness to EGF. By blocking STAT3 activity with the dominant-negative form, we show the requirement of STAT3 for EGF induction of MMP-1 and MMP-10 (stromelysin-2). Furthermore, expression of the dominant-negative STAT3 is sufficient to inhibit the constitutive and EGF-inducible cell migration and invasion and the tumor formation in nude mice. These results demonstrate that STAT3 phosphorylation and its possible interaction with c-JUN are required for the strong responsiveness of MMP-1 to EGF, and STAT3 activation is crucial for exhibition of malignant characteristics in T24 bladder cancer cells.

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“…Notably, the Stat3 pathway is activated in the gastrula organizer where it is thought to set up a signaling center that attracts lateral cells and thus promotes convergence toward the dorsal midline. Moreover, function of Stat3 is required in axial mesoderm cells for their anterior migration to drive extension (Yamashita et al, 2002Miyagi et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation

Sepich

Calmelet

Kiskowski

et al. 2005

Developmental Dynamics

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Embryonic morphogenesis is accomplished by cellular movements, rearrangements, and cell fate inductions. Vertebrate gastrulation entails morphogenetic processes that generate three germ layers, endoderm, mesoderm, and ectoderm, shaped into head, trunk, and tail. To understand how cell migration mechanistically contributes to tissue shaping during gastrulation, we examined migration of lateral mesoderm in the zebrafish. Our results illustrate that cell behaviors, different from mediolaterally oriented cell intercalation, also promote convergence and extension (C&E). During early gastrulation, upon internalization, individually migrating mesendodermal cells contribute to the elongation of the mesoderm by moving animally, without dorsal movement. Convergence toward dorsal starts later, by 70% epiboly (7.7 hpf). Depending on location along the Animal-Vegetal axis, an animal or vegetal bias is added to the dorsalward movement, so that paths fan out and the lateral mesoderm both converges and extends. Onset of convergence is independent of noncanonical Wnt signaling but is delayed when Stat3 signaling is compromised. To understand which aspects of motility are controlled by guidance cues, we measured turning behavior of lateral mesodermal cells. We show that cells exhibit directional preference, directionally-regulated speed, and turn toward dorsal when off-course. We estimate that ectoderm could supply from a fraction to all the dorsalward displacement seen in mesoderm cells. Using mathematical modeling, we demonstrate that directional preference is sufficient to account for mesoderm convergence and extension, and that, at minimum, two sources of guidance cues could orient cell paths realistically if located in the dorsal midline. Developmental Dynamics 234:279 -292, 2005.

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Stat3 Controls Cell Movements during Zebrafish Gastrulation

Cited by 171 publications

References 60 publications

Regulation of the early expression patterns of the zebrafish Dishevelled-interacting proteins Dapper1 and Dapper2

Regulation of the early expression patterns of the zebrafish Dishevelled-interacting proteins Dapper1 and Dapper2

Requirement of STAT3 activation for maximal collagenase-1 (MMP-1) induction by epidermal growth factor and malignant characteristics in T24 bladder cancer cells

Initiation of convergence and extension movements of lateral mesoderm during zebrafish gastrulation

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