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Competing activities of heterotrimeric G proteins in Drosophila wing maturation.

Katanayeva N, Kopein D, Portmann R, Hess D, Katanaev VL - PLoS ONE (2010)

Bottom Line: Loss of Gbeta13F, Ggamma1, or Galphas, but not any other G protein subunit, results in prevention of post-eclosion cell death and failure of the wing expansion.However, cell death prevention alone is not sufficient to induce the expansion defect, suggesting that the failure of epithelial-mesenchymal transition is key to the folded wing phenotypes.Our results provide a comprehensive functional analysis of the heterotrimeric G protein proteome in the late stages of Drosophila wing development.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Konstanz, Konstanz, Germany.

ABSTRACT
Drosophila genome encodes six alpha-subunits of heterotrimeric G proteins. The Galphas alpha-subunit is involved in the post-eclosion wing maturation, which consists of the epithelial-mesenchymal transition and cell death, accompanied by unfolding of the pupal wing into the firm adult flight organ. Here we show that another alpha-subunit Galphao can specifically antagonize the Galphas activities by competing for the Gbeta13F/Ggamma1 subunits of the heterotrimeric Gs protein complex. Loss of Gbeta13F, Ggamma1, or Galphas, but not any other G protein subunit, results in prevention of post-eclosion cell death and failure of the wing expansion. However, cell death prevention alone is not sufficient to induce the expansion defect, suggesting that the failure of epithelial-mesenchymal transition is key to the folded wing phenotypes. Overactivation of Galphas with cholera toxin mimics expression of constitutively activated Galphas and promotes wing blistering due to precocious cell death. In contrast, co-overexpression of Gbeta13F and Ggamma1 does not produce wing blistering, revealing the passive role of the Gbetagamma in the Galphas-mediated activation of apoptosis, but hinting at the possible function of Gbetagamma in the epithelial-mesenchymal transition. Our results provide a comprehensive functional analysis of the heterotrimeric G protein proteome in the late stages of Drosophila wing development.

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Overexpression of Gαo, but not other Gα-subunits, leads to the failure of wing expansion.Representative wings overexpressing Gαo (B), its activated form (Gαo[GTP], F), Gαi (C), Gαs (D), or Gαq (E) are shown along with the MS1096-Gal4 driver line alone (A).
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pone-0012331-g001: Overexpression of Gαo, but not other Gα-subunits, leads to the failure of wing expansion.Representative wings overexpressing Gαo (B), its activated form (Gαo[GTP], F), Gαi (C), Gαs (D), or Gαq (E) are shown along with the MS1096-Gal4 driver line alone (A).

Mentions: In the course of our studies of the role of the Gαo subunit of heterotrimeric G proteins in the Wnt and PCP signaling in Drosophila wing development [15] we came across an observation that overexpression of Gαo in Drosophila wings often led to the failure of wing expansion after fly hatching from the pupal case. Using the X-chromosome-located MS1096-Gal4 driver line, we found that ca. 80% of the aged adult female flies and 90% of male flies had folded wings characteristic of the freshly eclosed flies - a phenomenon never observed with wild-type animals (Fig. 1A, B, Table 2). MS1096-Gal4 drives strong expression in the dorsal domain and weaker expression in the ventral domain of the developing larval and pupal wing [25], [26], [27].


Competing activities of heterotrimeric G proteins in Drosophila wing maturation.

Katanayeva N, Kopein D, Portmann R, Hess D, Katanaev VL - PLoS ONE (2010)

Overexpression of Gαo, but not other Gα-subunits, leads to the failure of wing expansion.Representative wings overexpressing Gαo (B), its activated form (Gαo[GTP], F), Gαi (C), Gαs (D), or Gαq (E) are shown along with the MS1096-Gal4 driver line alone (A).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2925898&req=5

pone-0012331-g001: Overexpression of Gαo, but not other Gα-subunits, leads to the failure of wing expansion.Representative wings overexpressing Gαo (B), its activated form (Gαo[GTP], F), Gαi (C), Gαs (D), or Gαq (E) are shown along with the MS1096-Gal4 driver line alone (A).
Mentions: In the course of our studies of the role of the Gαo subunit of heterotrimeric G proteins in the Wnt and PCP signaling in Drosophila wing development [15] we came across an observation that overexpression of Gαo in Drosophila wings often led to the failure of wing expansion after fly hatching from the pupal case. Using the X-chromosome-located MS1096-Gal4 driver line, we found that ca. 80% of the aged adult female flies and 90% of male flies had folded wings characteristic of the freshly eclosed flies - a phenomenon never observed with wild-type animals (Fig. 1A, B, Table 2). MS1096-Gal4 drives strong expression in the dorsal domain and weaker expression in the ventral domain of the developing larval and pupal wing [25], [26], [27].

Bottom Line: Loss of Gbeta13F, Ggamma1, or Galphas, but not any other G protein subunit, results in prevention of post-eclosion cell death and failure of the wing expansion.However, cell death prevention alone is not sufficient to induce the expansion defect, suggesting that the failure of epithelial-mesenchymal transition is key to the folded wing phenotypes.Our results provide a comprehensive functional analysis of the heterotrimeric G protein proteome in the late stages of Drosophila wing development.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Konstanz, Konstanz, Germany.

ABSTRACT
Drosophila genome encodes six alpha-subunits of heterotrimeric G proteins. The Galphas alpha-subunit is involved in the post-eclosion wing maturation, which consists of the epithelial-mesenchymal transition and cell death, accompanied by unfolding of the pupal wing into the firm adult flight organ. Here we show that another alpha-subunit Galphao can specifically antagonize the Galphas activities by competing for the Gbeta13F/Ggamma1 subunits of the heterotrimeric Gs protein complex. Loss of Gbeta13F, Ggamma1, or Galphas, but not any other G protein subunit, results in prevention of post-eclosion cell death and failure of the wing expansion. However, cell death prevention alone is not sufficient to induce the expansion defect, suggesting that the failure of epithelial-mesenchymal transition is key to the folded wing phenotypes. Overactivation of Galphas with cholera toxin mimics expression of constitutively activated Galphas and promotes wing blistering due to precocious cell death. In contrast, co-overexpression of Gbeta13F and Ggamma1 does not produce wing blistering, revealing the passive role of the Gbetagamma in the Galphas-mediated activation of apoptosis, but hinting at the possible function of Gbetagamma in the epithelial-mesenchymal transition. Our results provide a comprehensive functional analysis of the heterotrimeric G protein proteome in the late stages of Drosophila wing development.

Show MeSH
Related in: MedlinePlus