DSH-2 regulates asymmetric cell division in the early C. elegans somatic gonad

Weiru Chang; Christine E. Lloyd; David Zarkower

doi:10.1016/j.mod.2005.03.005

DSH-2 regulates asymmetric cell division in the early C. elegans somatic gonad

Weiru Chang, Christine E. Lloyd, David Zarkower

Genetics, Cell Biology and Development (TMED)

Research output: Contribution to journal › Article › peer-review

24 Scopus citations

Abstract

Like other organs, the C. elegans gonad develops from a simple primordium that must undergo axial patterning to generate correct adult morphology. Proximal/distal (PD) polarity in the C. elegans gonad is established early during gonadogenesis by the somatic gonad precursor cells, Z1 and Z4. Z1 and Z4 each divide asymmetrically to generate one daughter with a proximal fate and one with a distal fate. PD polarity of the Z1/Z4 lineages requires the activity of a Wnt pathway that activates the TCF/LEF homolog pop-1. How the gonadal pathway controlling pop-1 is regulated by upstream factors has been unclear, as neither Wnt nor Dishevelled (Dsh) proteins have been shown to be required. Here we show that the C. elegans dsh homolog dsh-2 controls gonadal polarity. As in pop-1 mutants, dsh-2 hermaphrodites have Z1 and Z4 lineage defects indicative of defective PD polarity and are missing gonadal arms. Males have an elongated but disorganized gonad, also with lineage defects. DSH-2 protein is expressed in the Z1/Z4 gonadal precursor cells. Asymmetric distribution of nuclear GFP::POP-1 in Z1 and Z4 daughter cells is reversed in dsh-2 mutants, with higher levels in distal than proximal daughters. dsh-2 and the frizzled receptor homolog lin-17 have a strong genetic interaction, suggesting that they act in a common pathway. We suggest that DSH-2 functions as an upstream regulator of POP-1 in the somatic gonad to control asymmetric cell division, thereby establishing proximal-distal polarity of the developing organ.

Original language	English (US)
Pages (from-to)	781-789
Number of pages	9
Journal	Mechanisms of Development
Volume	122
Issue number	6
DOIs	https://doi.org/10.1016/j.mod.2005.03.005
State	Published - Jun 2005

Bibliographical note

Funding Information:
The authors thank Gregory Ellis, Bruce Bowerman, Nancy Hawkins, Gian Garriga, Jeff Hardin, Trey Kidd, and Judith Kimble for generously providing reagents, in some cases prior to publication, and for helpful advice. We thank Michael Herman for critical reading of the manuscript and members of the Zarkower lab for helpful discussions. This work was supported by a grant to D.Z. (GM53099) and a predoctoral training grant to W.C. (HD07480).

Keywords

Asymmetry
C. elegans
Cell fate
Dishevelled
Somatic gonad
Wnt
pop-1

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title = "DSH-2 regulates asymmetric cell division in the early C. elegans somatic gonad",

abstract = "Like other organs, the C. elegans gonad develops from a simple primordium that must undergo axial patterning to generate correct adult morphology. Proximal/distal (PD) polarity in the C. elegans gonad is established early during gonadogenesis by the somatic gonad precursor cells, Z1 and Z4. Z1 and Z4 each divide asymmetrically to generate one daughter with a proximal fate and one with a distal fate. PD polarity of the Z1/Z4 lineages requires the activity of a Wnt pathway that activates the TCF/LEF homolog pop-1. How the gonadal pathway controlling pop-1 is regulated by upstream factors has been unclear, as neither Wnt nor Dishevelled (Dsh) proteins have been shown to be required. Here we show that the C. elegans dsh homolog dsh-2 controls gonadal polarity. As in pop-1 mutants, dsh-2 hermaphrodites have Z1 and Z4 lineage defects indicative of defective PD polarity and are missing gonadal arms. Males have an elongated but disorganized gonad, also with lineage defects. DSH-2 protein is expressed in the Z1/Z4 gonadal precursor cells. Asymmetric distribution of nuclear GFP::POP-1 in Z1 and Z4 daughter cells is reversed in dsh-2 mutants, with higher levels in distal than proximal daughters. dsh-2 and the frizzled receptor homolog lin-17 have a strong genetic interaction, suggesting that they act in a common pathway. We suggest that DSH-2 functions as an upstream regulator of POP-1 in the somatic gonad to control asymmetric cell division, thereby establishing proximal-distal polarity of the developing organ.",

keywords = "Asymmetry, C. elegans, Cell fate, Dishevelled, Somatic gonad, Wnt, pop-1",

author = "Weiru Chang and Lloyd, {Christine E.} and David Zarkower",

note = "Funding Information: The authors thank Gregory Ellis, Bruce Bowerman, Nancy Hawkins, Gian Garriga, Jeff Hardin, Trey Kidd, and Judith Kimble for generously providing reagents, in some cases prior to publication, and for helpful advice. We thank Michael Herman for critical reading of the manuscript and members of the Zarkower lab for helpful discussions. This work was supported by a grant to D.Z. (GM53099) and a predoctoral training grant to W.C. (HD07480).",

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AU - Lloyd, Christine E.

AU - Zarkower, David

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PY - 2005/6

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N2 - Like other organs, the C. elegans gonad develops from a simple primordium that must undergo axial patterning to generate correct adult morphology. Proximal/distal (PD) polarity in the C. elegans gonad is established early during gonadogenesis by the somatic gonad precursor cells, Z1 and Z4. Z1 and Z4 each divide asymmetrically to generate one daughter with a proximal fate and one with a distal fate. PD polarity of the Z1/Z4 lineages requires the activity of a Wnt pathway that activates the TCF/LEF homolog pop-1. How the gonadal pathway controlling pop-1 is regulated by upstream factors has been unclear, as neither Wnt nor Dishevelled (Dsh) proteins have been shown to be required. Here we show that the C. elegans dsh homolog dsh-2 controls gonadal polarity. As in pop-1 mutants, dsh-2 hermaphrodites have Z1 and Z4 lineage defects indicative of defective PD polarity and are missing gonadal arms. Males have an elongated but disorganized gonad, also with lineage defects. DSH-2 protein is expressed in the Z1/Z4 gonadal precursor cells. Asymmetric distribution of nuclear GFP::POP-1 in Z1 and Z4 daughter cells is reversed in dsh-2 mutants, with higher levels in distal than proximal daughters. dsh-2 and the frizzled receptor homolog lin-17 have a strong genetic interaction, suggesting that they act in a common pathway. We suggest that DSH-2 functions as an upstream regulator of POP-1 in the somatic gonad to control asymmetric cell division, thereby establishing proximal-distal polarity of the developing organ.

AB - Like other organs, the C. elegans gonad develops from a simple primordium that must undergo axial patterning to generate correct adult morphology. Proximal/distal (PD) polarity in the C. elegans gonad is established early during gonadogenesis by the somatic gonad precursor cells, Z1 and Z4. Z1 and Z4 each divide asymmetrically to generate one daughter with a proximal fate and one with a distal fate. PD polarity of the Z1/Z4 lineages requires the activity of a Wnt pathway that activates the TCF/LEF homolog pop-1. How the gonadal pathway controlling pop-1 is regulated by upstream factors has been unclear, as neither Wnt nor Dishevelled (Dsh) proteins have been shown to be required. Here we show that the C. elegans dsh homolog dsh-2 controls gonadal polarity. As in pop-1 mutants, dsh-2 hermaphrodites have Z1 and Z4 lineage defects indicative of defective PD polarity and are missing gonadal arms. Males have an elongated but disorganized gonad, also with lineage defects. DSH-2 protein is expressed in the Z1/Z4 gonadal precursor cells. Asymmetric distribution of nuclear GFP::POP-1 in Z1 and Z4 daughter cells is reversed in dsh-2 mutants, with higher levels in distal than proximal daughters. dsh-2 and the frizzled receptor homolog lin-17 have a strong genetic interaction, suggesting that they act in a common pathway. We suggest that DSH-2 functions as an upstream regulator of POP-1 in the somatic gonad to control asymmetric cell division, thereby establishing proximal-distal polarity of the developing organ.

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KW - C. elegans

KW - Cell fate

KW - Dishevelled

KW - Somatic gonad

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AN - SCOPUS:20444369232

SN - 0925-4773

VL - 122

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JO - Mechanisms of Development

JF - Mechanisms of Development

IS - 6

ER -

DSH-2 regulates asymmetric cell division in the early C. elegans somatic gonad

Abstract

Bibliographical note

Keywords

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