C. elegans LIN-18 Is a Ryk Ortholog and Functions in Parallel to LIN-17/Frizzled in Wnt Signaling

Inoué, Takao; Oz, Helieh S.; Wiland, Debra; Gharib, Shahla; Deshpande, Rashmi; Hill, Russell J.; Katz, Wendy S.; Sternberg, Paul W.

doi:10.1016/j.cell.2004.09.001

Cited by 175 publications

(185 citation statements)

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“…1 F and G) (26), cog-1 and lin-11, in turn, control the expression pattern of egl-17 and cdh-3. Patterns of egl-17 and cdh-3 expression observed in lin-17 and lin-18 mutants are consistent with high levels of cog-1 and lin-11 turning on the expression of these genes (31,32). Another set of cell-fatepatterning mechanisms controlling gene expression was revealed by the analysis of vulE vs. vulF fate specification using the zmp-1 reporter.…”

Section: Resultsmentioning

confidence: 73%

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Transcriptional network underlying Caenorhabditis elegans vulval development

Inoué

Wang

Ririe

et al. 2005

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

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The vulval development of Caenorhabditis elegans provides an opportunity to investigate genetic networks that control gene expression during organogenesis. During the fourth larval stage (L4), seven vulval cell types are produced, each of which executes a distinct gene expression program. We analyze how the expression of cell-type-specific genes is regulated. Ras and Wnt signaling pathways play major roles in generating the spatial pattern of cell types and regulate gene expression through a network of transcription factors. One transcription factor (lin-29) primarily controls the temporal expression pattern. Other transcription factors (lin-11, cog-1, and egl-38) act in combination to control cell-typespecific gene expression. The complexity of the network arises in part because of the dynamic nature of gene expression, in part because of the presence of seven cell types, and also because there are multiple regulatory paths for gene expression within each cell type.organogenesis ͉ signaling pathways ͉ transcription D evelopmental events are driven by spatially and temporally regulated gene expression. Understanding how complex patterns of expression are produced is therefore a critical part of deciphering mechanisms of development. In general, intercellular signaling mechanisms interact with a network of transcription factors to generate cell-type-specific patterns of gene expression. The late stage of Caenorhabditis elegans vulval development offers a useful model in which to study this process. During this period of vulval development, seven distinct cell types are produced that express unique combinations of genes. Over the last several years, a number of genes were discovered that are expressed in cell-type and stage-specific patterns in the vulva, and several transcription factors were found to regulate these genes. In this paper, we synthesize and extend our current knowledge of this genetic network.The C. elegans vulva connects the uterine lumen to the outside, allowing for passage of sperm and fertilized eggs (1). Vulval cells are generated postembryonically from precursor cells P3.p P4.p, P5.p, P6.p, P7.p, and P8.p [also called vulval precursor cells (VPC)]. During the mid-third larval (L3) stage, EGF and Notch signaling induces the middle three VPCs (P5.p, P6.p, and P7.p) to adopt vulval fates, whereas P3.p, P4.p, and P8.p fuse with the hypodermal syncytium, hyp7 (2-6).During the late-L3 to the early-L4 stage, P5.p, P6.p, and P7.p undergo two or three rounds of cell division to produce 22 nuclei (7) (Fig. 1A). These nuclei are in cells of seven types (vulA, vulB1, vulB2, vulC, vulD, vulE, and vulF), as evidenced by subsequent morphogenetic movements and by the pattern of gene expression (8, 9) (Fig. 1B). The seven cell types that are present in the adult vulva represent specializations within the general epithelial cell class. These cells exhibit cell-type general features; for example, each expresses ajm-1, a component of the apical junction that connects neighboring cells in epithelial tissues (8)....

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Section: Resultsmentioning

confidence: 73%

“…1 A). Although the full mechanism that establishes this pattern is not known, Wnt signals, mediated by lin-17 (Frizzled-type Wnt receptor) and lin-18 (Ryk-type Wnt receptor), control the anterior͞posterior order of cell types among P7.p descendants (31,32) (Fig. 3).…”

Section: Resultsmentioning

confidence: 99%

Transcriptional network underlying Caenorhabditis elegans vulval development

Inoué

Wang

Ririe

et al. 2005

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

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“…It has previously been shown that the Wnt pathway is involved in the generation of the P. pacificus vulva (13,14,22). In a similar fashion, in C. elegans, Wnt signaling is also required at different times in development to generate both a functional gonad and a functional vulva (15,16,(23)(24)(25)(26). Although the exact roles in specific cell-fate decisions within these lineages are likely to be quite different between P. pacificus and C. elegans, it is tempting to speculate that alterations in the timing and spatial expression of Wnt ligands or Frizzled receptors in vulval and gonadal lineages, respectively, may be responsible for the change in organ shape that we describe here.…”

Section: Discussionmentioning

confidence: 92%

Wnt signaling in Pristionchus pacificus gonadal arm extension and the evolution of organ shape

Rudel

Tian

Sommer

2008

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

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Changes in organ morphology have been essential to the evolution of novel body forms and in permitting organisms to invade new ecological niches. Changes in the arrangement of cells and tissues and in the regulation of morphological movements are fundamental to evolutionary transitions of organ shape and function. However, little is known about the genetic and developmental control of these changes. We use interspecific differences in the migration and extension of the nematode hermaphrodite gonadal arms to study the generation of morphological novelty. We show that the extending Pristionchus pacificus gonadal arms display a ventral migration that is unique to the Diplogastridae in comparison to the Rhabditidae, including Caenorhabditis elegans, and other nematodes. This results in the distal gonad residing along the ventral side of the body in P. pacificus in contrast to lying on the dorsal side of the body as in C. elegans. We show that at the cellular level this morphogenetic movement is regulated by signals from the developing vulva and the sister gonadal arm. We further show that in P. pacificus Wnt signaling is essential for this regulation. We show genetic and molecular evidence that suggest the Wnt ligands Ppa-mom-2 and Ppa-cwn-2 are components of the signaling mechanism. Supporting these findings, the hermaphrodite gonad of Ppa-bar-1 mutant animals mimics the shape of the C. elegans hermaphrodite gonad; the arms fail to extend ventrally. Thus, this genetic analysis of gonad migration provides insight into the mechanisms underlying the generation of morphological novelty and organ shape.development ͉ gonad ͉ nematode

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“…Two major classes of receptors mediate Wnt action, Frizzleds and Ryk/Derailed. Both classes of receptors are also involved in earlier functions, such as cell fate determination (Wodarz and Nusse, 1998;Halford et al, 2000;Inoue et al, 2004). There is no compelling evidence that Drosophila frizzled genes interact with derailed (Yoshikawa et al, 2003).…”

Section: Specificitymentioning

confidence: 99%