Gbx2 interacts with Otx2 and patterns the anterior–posterior axis during gastrulation in Xenopus

Tour, Ella; Pillemer, Graciela; Gruenbaum, Yosef; Fainsod, Abraham

doi:10.1016/s0925-4773(01)00653-0

Cited by 38 publications

(36 citation statements)

References 70 publications

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“…In frogs, Otx has been shown to negatively regulate convergent extension movements through Calponin (34). A subdivision into an anterior otx-and a posteriorly adjacent gbx-expressing region is of widespread occurrence in developing bilaterians (1,(35)(36)(37)(38), but a spatial correlation to the anteroposterior extent of convergent extension has not been documented except for vertebrates.…”

Section: An Otx-gbx Morphogenetic Boundary Anteriorly Delimitates Thementioning

confidence: 99%

Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation

Steinmetz

Zelada-Gonzáles

Burgtorf

et al. 2007

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

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During frog and fish development, convergent extension movements transform the spherical gastrula into an elongated neurula. Such transformation of a ball-into a worm-shaped embryo is an ancestral and fundamental feature of bilaterian development, yet this is modified or absent in the protostome model organisms Caenorhabditis or Drosophila. In the polychaete annelid Platynereis dumerilii, early embryonic and larval stages resemble a sphere that subsequently elongates into worm shape. Cellular and molecular mechanisms of polychaete body elongation are yet unknown. Our in vivo time-lapse analysis of Platynereis axis elongation reveals that the polychaete neuroectoderm converges and extends by mediolateral cell intercalation. This occurs on both sides of the neural midline, the line of fusion of the slit-like blastopore. Convergent extension moves apart mouth and anus that are both derived from the blastopore. Tissue elongation is actin-dependent but microtubule-independent. Dependence on JNK activity and spatially restricted expression of strabismus indicates involvement of the noncanonical Wnt pathway. We detect a morphogenetic boundary between the converging and extending trunk neuroectoderm and the anterior otx-expressing head neuroectoderm that does not elongate. Our comparative analysis uncovers striking similarities but also differences between convergent extension in the polychaete and in the frog (the classical vertebrate model for convergent extension). Based on these findings, we propose that convergent extension movements of the trunk neuroectoderm represent an ancestral feature of bilaterian development that triggered the separation of mouth and anus along the elongating trunk.amphistomy ͉ axis formation ͉ convergent extension ͉ gastrulation

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Section: An Otx-gbx Morphogenetic Boundary Anteriorly Delimitates Thementioning

confidence: 99%

Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation

Steinmetz

Zelada-Gonzáles

Burgtorf

et al. 2007

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

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“…In addition, gain-of-function experiments showed that mis-expression of Gbx2 in the midbrain causes repression of Otx2 and anterior expansion of r1 (Katahira et al, 2000;Kikuta et al, 2003;Millet et al, 1999;Tour et al, 2002), and that this is dependent on the repressor function of Gbx2 (Tour et al, 2002). However, Gbx2 also has been shown to function as a transcriptional activator in certain cellular contexts (Kowenz-Leutz et al, 1997).…”

Section: Gbx2 Is Not Sufficient To Induce a Cerebellummentioning

confidence: 99%

New regulatory interactions and cellular responses in the isthmic organizer region revealed by alteringGbx2expression

Lao

Joyner

2005

Development

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The mouse homeobox gene Gbx2 is first expressed throughout the posterior region of the embryo during gastrulation, and becomes restricted to rhombomeres 1-3 (r1-3) by embryonic day 8.5 (E8.5). Previous studies have shown that r1-3 do not develop in Gbx2 mutants and that there is an early caudal expansion of the midbrain gene Otx2 to the anterior border of r4. Furthermore, expression of Wnt1 and Fgf8, two crucial components of the isthmic organizer, is no longer segregated to adjacent domains in Gbx2 mutants. In this study, we extend the phenotypic analysis of Gbx2 mutants by showing that Gbx2 is not only required for development of r1-3, but also for normal gene expression in r4-6. To determine whether Gbx2 can alter hindbrain development, we generated Hoxb1-Gbx2 (HG) transgenic mice in which Gbx2 is ectopically expressed in r4. We show that Gbx2 is not sufficient to induce r1-3 development in r4. To test whether an Otx2/Gbx2 interface can induce r1-3 development, we introduced the HG transgene onto a Gbx2-null mutant background and recreated a new Otx2/Gbx2 border in the anterior hindbrain. Development of r3, but not r1 and r2, is rescued in Gbx2–/–; HG embryos. In addition, the normal spatial relationship of Wnt1 and Fgf8 is established at the new Otx2/Gbx2 border, demonstrating that an interaction between Otx2 and Gbx2 is sufficient to produce the normal pattern of Wnt1 and Fgf8 expression. However, the expression domains of Fgf8 and Spry1, a downstream target of Fgf8, are greatly reduced in mid/hindbrain junction area of Gbx2–/–; HG embryos and the posterior midbrain is truncated because of abnormal cell death. Interestingly, we show that increased cell death and a partial loss of the midbrain are associated with increased expression of Fgf8 and Spry1 in Gbx2conditional mutants that lack Gbx2 in r1 after E9.0. These results together suggest that cell survival in the posterior midbrain is positively or negatively regulated by Fgf8, depending on Fgf8 expression level. Our studies provide new insights into the regulatory interactions that maintain isthmic organizer gene expression and the consequences of altered levels of organizer gene expression on cell survival.

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“…In vertebrates, both Fgf8 and Gbx2 have a repressive activity on Otx2 expression in the metencephalic alar plate (Liu and Joyner, 1999;Martinez et al, 1999;Millet et al, 1999;Tour et al, 2002). In addition, zebrafish gbx2 is fully dependent on Fgf8 during the maintenance period (Rhinn et al, 2003).…”

Section: Possible Molecular Mechanisms Underlying the Isthmus-to-midbmentioning

confidence: 99%

Isthmus-to-midbrain transformation in the absence of midbrain-hindbrain organizer activity

et al. 2003

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In zebrafish acerebellar (ace) embryos, because of a point mutation in fgf8, the isthmic constriction containing the midbrain-hindbrain boundary (MHB) organizer fails to form. The mutants lack cerebellar development by morphological criteria, and they appear to have an enlarged tectum, showing no obvious reduction in the tissue mass at the dorsal mesencephalic/metencephalic alar plate. To reveal the molecular identity of the tissues located at equivalent rostrocaudal positions along the neuraxis as the isthmic and cerebellar primordia in wild-types, we undertook a detailed analysis of ace embryos. In ace mutants, the appearance of forebrain and midbrain specific marker genes (otx2, dmbx1, wnt4) in the caudal tectal enlargement reveals a marked rostralized gene expression profile during early somitogenesis, followed by the lack of early and late cerebellar-specific gene expression (zath1/atoh1, gap43,tag1/cntn2, neurod, zebrin II). The Locus coeruleus(LC) derived from rostral rhombomere 1 is also absent in the mutants. A new interface between otx2 and epha4a suggests that the rostralization stops at the caudal part of rhombomere 1. The mesencephalic basal plate is also affected in the mutant embryos, as indicated by the caudal expansion of the diencephalic expression domains of epha4a,zash1b/ashb, gap43 and tag1/cntn2, and by the dramatic reduction of twhh expression. No marked differences are seen in cell proliferation and apoptotic patterns around the time the rostralization of gene expression becomes evident in the mutants. Therefore,locally distinct cell proliferation and cell death is unlikely to be the cause of the fate alteration of the isthmic and cerebellar primordia in the mutants. Dil cell-lineage labeling of isthmic primordial cells reveals that cells, at the location equivalent of the wild-type MHB, give rise to caudal tectum in ace embryos. This suggests that a caudalto-rostral transformation leads to the tectal expansion in the mutants. Fgf8-coated beads are able to rescue morphological MHB formation, and elicit the normal molecular identity of the isthmic and cerebellar primordium in ace embryos. Taken together, our analysis reveals that cells of the isthmic and cerebellar primordia acquire a more rostral, tectal identity in the absence of the functional MHB organizer signal Fgf8.

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Gbx2 interacts with Otx2 and patterns the anterior–posterior axis during gastrulation in Xenopus

Cited by 38 publications

References 70 publications

Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation

Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation

New regulatory interactions and cellular responses in the isthmic organizer region revealed by alteringGbx2expression

Isthmus-to-midbrain transformation in the absence of midbrain-hindbrain organizer activity

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