Fusomorphogenesis: Cell fusion in organ formation

Shemer, Gidi; Podbilewicz, Benjamin

doi:10.1002/(sici)1097-0177(200005)218:1<30::aid-dvdy4>3.0.co;2-w

Cited by 66 publications

(42 citation statements)

References 152 publications

(183 reference statements)

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“…In C. elegans, most epidermal (also known as hypodermal) cells fuse to form multinucleate syncytia, which play essential roles in protecting the animal's body by secreting collagens that make up the cuticle surrounding the body (36); in regulating cell fate specification of the neighboring cells, including the seam cells and the Pn.p cells (see below) (23,46); and in taking up dietary sterols (69). A major epidermal syncytium, hyp7, is formed by the fusion of Ͼ100 cells, and it covers the majority of the animal's body (55). Our study revealed that nhr-25 mutants display defects in the ventral epidermal cells in embryos and in the epidermal syncytial cells, the seam cells, and the Pn.p cells in larvae.…”

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confidence: 66%

The Caenorhabditis elegans Nuclear Receptor Gene nhr-25 Regulates Epidermal Cell Development

Chen

Eastburn

Han

2004

Molecular and Cellular Biology

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The development of the epidermis of Caenorhabditis elegans involves cell fusion, migration, and differentiation events. To understand the mechanisms underlying these processes, we characterized the roles of NHR-25, a member of the nuclear receptor family of transcription factors. The NHR-25 homologs Ftz-F1 in Drosophila and SF-1 in mammals are involved in various biological processes, including regulation of patterning during development, reproduction, metabolism, metamorphosis, and homeostasis. Impairment of nhr-25 activity leads to severe phenotypes in embryos and many postembryonic tissues. Further analysis has indicated that nhr-25 activity is required for the proper development, including cell-cell fusion, of several epidermal cell types, such as the epidermal syncytial, seam, and Pn.p cells. Our results also suggest that nhr-25 is likely to regulate cell-cell junctions and/or fusion. In a subset of Pn.p cells, called vulval precursor cells, nhr-25 acts collaboratively with the lin-39 Hox gene in regulating vulval cell differentiation. Additionally, our data suggest that nhr-25 may also function with another Hox gene, nob-1, during embryogenesis. Overall, our results indicate that nhr-25 plays an integral role in regulating cellular processes of epidermal cells.Members of the nuclear receptor (NR) superfamily of transcription factors (also known as nuclear hormone receptors [NHRs]) share some highly conserved peptide motifs, including DNA-binding, ligand-binding, and transactivation domains (for a review, see reference 44). However, these proteins carry out diverse physiological functions (for a review, see references 8, 44, and 60). As more NRs have been identified, the features of the ligands for these receptors have been shown to be more chemically diverse, and not exclusively endocrine (for a review, see references 8 and 15). For many of the identified NRs, no apparent ligands have been found, and these proteins are therefore referred to as orphan nuclear receptors (for a review, see references 8 and 43).Members of one subfamily of the orphan receptors bind to nonrepetitive DNA sequences as monomers and are constitutively localized to the nucleus; these members include Drosophila ␣Ftz-F1 (fushi tarazu factor 1) and mammalian SF-1 (steroidogenic factor 1) (42). Previous studies of Drosophila have shown that ␣Ftz-F1 functions collaboratively with a homeodomain protein, fushi tarazu (Ftz), to promote cell fate specification in fly embryos (25, 70). Mutations in ftz or ␣ftz-f1 cause a common pair rule phenotype, which is associated with defects in alternate segments of the embryos. The alternatively spliced ␤ isoform of Ftz-F1 has been found to regulate ecdysone-induced gene expression and therefore is involved in the metamorphosis of flies (4). Mammalian homologues of ftz-f1 include the SF-1 and LRH-1 (liver receptor homologue 1) proteins. SF-1 functions in regulating the transcription of some steroidogenic enzymes and plays an essential role in the development of the adrenal gland and gonad (28,30,37). LR...

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confidence: 66%

The Caenorhabditis elegans Nuclear Receptor Gene nhr-25 Regulates Epidermal Cell Development

Chen

Eastburn

Han

2004

Molecular and Cellular Biology

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“…The underlying defect in these instances seems to be improper formation of the hyp5 hypodermal syncytium (Figure 8). During morphogenesis of the anterior hypodermis (reviewed in Shemer and Podbilewicz, 2000;Piekny and Mains, 2003), cells from the dorsal side of the embryo extend to meet at the ventral midline. Subsequent fusion between specific cells produces the toroidal-shaped cells that enclose the head of the embryo.…”

Section: Discussionmentioning

confidence: 99%

“…This phenotype is reminiscent of that described previously for strains defective in morphogenesis of the anterior hypodermis (Brenner, 1974;Wang et al, 1999;Ginzburg et al, 2002). The morphogenesis of the C. elegans hypodermis occurs during embryogenesis (reviewed in Shemer and Podbilewicz, 2000;Piekny and Mains, 2003). The hypodermal precursors are initially positioned as a sheet of cells resting on the dorsal surface of the embryo.…”

Section: Alr-1 Mutants Display Defects In Anterior Hypodermal Morphogmentioning

confidence: 99%

TheCaenorhabditis elegans aristalessOrthologue,alr-1, Is Required for Maintaining the Functional and Structural Integrity of the Amphid Sensory Organs

Tucker

Sieber

Morphew

et al. 2005

MBoC

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The homeobox-containing aristaless-related protein ARX has been directly linked to the development of a number of human disorders involving mental retardation and epilepsy and clearly plays a critical role in development of the vertebrate central nervous system. In this work, we investigate the role of ALR-1, the Caenorhabditis elegans aristaless orthologue, in amphid sensory function. Our studies indicate that ALR-1 is required for maintenance of the amphid organ structure throughout larval development. Mutant analysis indicates a progressive loss in the amphid neurons' ability to fill with lipophilic dyes as well as a declining chemotactic response. The degeneration in amphid function corresponds with a failure of the glial-like amphid socket cell to maintain its specific cell shape and cell-cell contacts. Consistent with ALR-1 expression within the amphid socket cell, our results indicate a cell autonomous role for ALR-1 in maintaining cell shape. Furthermore, we demonstrate a role for ALR-1 in the proper morphogenesis of the anterior hypodermis. Genetic interaction tests also suggest that ALR-1 may function cooperatively with the cell adhesion processes in maintaining the amphid sensory organs.

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“…During this process, the embryo changes from a shape resembling a lima bean to a long, thin shape of a worm. During this process the membranes of the hypodermal cells fuse in a reproducible sequence to form cylindrical syncytial cells linked to each other by the CeAJ (Chin-Sang and Chisholm, 2000;Shemer and Podbilewicz, 2000). Previous analysis of live epidermal cell fusion has shown that dissolution of the CeAJ takes place shortly after plasma membranes have disappeared between two fusing cells (Mohler et al, 1998).…”

Section: Epidermal Development In C Elegansmentioning

confidence: 99%

Molecular networks controlling epithelial cell polarity in development

Müller

Bossinger

2003

Mechanisms of Development

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During embryonic development, polarized epithelial cells are either formed during cleavage or formed from mesenchymal cells. Because the formation of epithelia during embryogenesis has to occur with high fidelity to ensure proper development, embryos allow a functional approach to study epithelial cell polarization in vivo. In particular, genetic model organisms have greatly advanced our understanding of the generation and maintenance of epithelial cell polarity. Many novel and important polarity genes have been identified and characterized in invertebrate systems, like Drosophila melanogaster and Caenorhabditis elegans. With the rapid identification of mammalian homologues of these invertebrate polarity genes, it has become clear that many important protein domains, single proteins and even entire protein complexes are evolutionarily conserved. It is to be expected that the field of epithelial cell polarity is just experiencing the 'top of the iceberg' of a large protein network that is fundamental for the specific adhesive, cell signalling and transport functions of epithelial cells.

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Fusomorphogenesis: Cell fusion in organ formation

Cited by 66 publications

References 152 publications

The Caenorhabditis elegans Nuclear Receptor Gene nhr-25 Regulates Epidermal Cell Development

The Caenorhabditis elegans Nuclear Receptor Gene nhr-25 Regulates Epidermal Cell Development

TheCaenorhabditis elegans aristalessOrthologue,alr-1, Is Required for Maintaining the Functional and Structural Integrity of the Amphid Sensory Organs

Molecular networks controlling epithelial cell polarity in development

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