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The prickle-Related Gene in Vertebrates Is Essential for Gastrulation Cell Movements

2003; Elsevier BV; Volume: 13; Issue: 8 Linguagem: Inglês

10.1016/s0960-9822(03)00245-8

1879-0445

Masaki Takeuchi, Jun Nakabayashi, Takuya Sakaguchi, Takamasa Yamamoto, Hiroki Takahashi, Hiroyuki Takeda, Naoto Ueno,

Hippo pathway signaling and YAP/TAZ

Involving dynamic and coordinated cell movements that cause drastic changes in embryo shape, gastrulation is one of the most important processes of early development. Gastrulation proceeds by various types of cell movements, including convergence and extension, during which polarized axial mesodermal cells intercalate in radial and mediolateral directions and thus elongate the dorsal marginal zone along the anterior-posterior axis [1Shih J. Keller R. Cell motility driving mediolateral intercalation in explants of Xenopus laevis.Development. 1992; 116: 901-914Crossref PubMed Google Scholar, 2Wilson P. Keller R. Cell rearrangement during gastrulation of Xenopusdirect observation of cultured explants.Development. 1991; 112: 289-300PubMed Google Scholar]. Recently, it was reported that a noncanonical Wnt signaling pathway, which is known to regulate planar cell polarity (PCP) in Drosophila[3Adler P.N. The genetic control of tissue polarity in Drosophila.Bioessays. 1992; 14: 735-741Crossref PubMed Scopus (153) Google Scholar, 4Mlodzik M. Planar polarity in the Drosophila eye a multifaceted view of signaling specificity and cross-talk.EMBO J. 1999; 18: 6873-6879Crossref PubMed Scopus (145) Google Scholar], participates in the regulation of convergent extension movements in Xenopus as well as in the zebrafish embryo [5Djiane A. Riou J. Umbhauer M. Boucaut J. Shi D. Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis.Development. 2000; 127: 3091-3100PubMed Google Scholar, 6Heisenberg C.P. Tada M. Rauch G.J. Saude L. Concha M.L. Geisler R. Stemple D.L. Smith J.C. Wilson S.W. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation.Nature. 2000; 405: 76-81Crossref PubMed Scopus (791) Google Scholar, 7Tada M. Smith J.C. Xwnt11 is a target of Xenopus Brachyury regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway.Development. 2000; 127: 2227-2238Crossref PubMed Google Scholar, 8Wallingford J.B. Rowning B.A. Vogeli K.M. Rothbacher U. Fraser S.E. Harland R.M. Dishevelled controls cell polarity during Xenopus gastrulation.Nature. 2000; 405: 81-85Crossref PubMed Scopus (606) Google Scholar]. The Wnt5a/Wnt11 signal is mediated by members of the seven-pass transmembrane receptor Frizzled (Fz) and the signal transducer Dishevelled (Dsh) through the Dsh domains that are required for the PCP signal [6Heisenberg C.P. Tada M. Rauch G.J. Saude L. Concha M.L. Geisler R. Stemple D.L. Smith J.C. Wilson S.W. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation.Nature. 2000; 405: 76-81Crossref PubMed Scopus (791) Google Scholar, 7Tada M. Smith J.C. Xwnt11 is a target of Xenopus Brachyury regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway.Development. 2000; 127: 2227-2238Crossref PubMed Google Scholar, 8Wallingford J.B. Rowning B.A. Vogeli K.M. Rothbacher U. Fraser S.E. Harland R.M. Dishevelled controls cell polarity during Xenopus gastrulation.Nature. 2000; 405: 81-85Crossref PubMed Scopus (606) Google Scholar]. It has also been shown that the relocalization of Dsh to the cell membrane is required for convergent extension movements in Xenopus gastrulae. Although it appears that signaling via these components leads to the activation of JNK [9Boutros M. Paricio N. Strutt D.I. Mlodzik M. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling.Cell. 1998; 94: 109-118Abstract Full Text Full Text PDF PubMed Scopus (643) Google Scholar, 10Yamanaka H. Moriguchi T. Masuyama N. Kusakabe M. Hanafusa H. Takada R. Takada S. Nishida E. JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates.EMBO Rep. 2002; 3: 69-75Crossref PubMed Scopus (337) Google Scholar] and rearrangement of microtubules, the precise interplay among these intercellular components is largely unknown. In this study, we show that Xenopus prickle (Xpk), a Xenopus homolog of a Drosophila PCP gene [11Gubb D. Green C. Huen D. Coulson D. Johnson G. Tree D. Collier S. Roote J. The balance between isoforms of the prickle LIM domain protein is critical for planar polarity in Drosophila imaginal discs.Genes Dev. 1999; 13: 2315-2327Crossref PubMed Scopus (212) Google Scholar, 12Mlodzik M. Spiny legs and prickled bodies new insights and complexities in planar polarity establishment.Bioessays. 2000; 22: 311-315Crossref PubMed Scopus (26) Google Scholar, 13Tree D.R. Shulman J.M. Rousset R. Scott M.P. Gubb D. Axelrod J.D. Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling.Cell. 2002; 109: 371-381Abstract Full Text Full Text PDF PubMed Scopus (327) Google Scholar], is an essential component for gastrulation cell movement. Both gain-of-function and loss-of-function of Xpk severely perturbed gastrulation and caused spina bifida embryos without affecting mesodermal differentiation. We also demonstrate that XPK binds to Xenopus Dsh as well as to JNK. This suggests that XPK plays a pivotal role in connecting Dsh function to JNK activation.