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Transition zone assembly and its contribution to axoneme formation in Drosophila male germ cells

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ABSTRACT

Ciliary transition zone (TZ) assembly is complex and incompletely understood. Vieillard et al. show that Drosophila Cby and Dila cooperate to assemble the TZ and membrane cap, which, together with microtubule remodeling by kinesin-13, is required for axoneme formation in male germ cells.

No MeSH data available.


TZ components in Drosophila and scheme of spermatogenesis. (A) Scheme of TZ components present in mammals assigned in different functional modules. Conserved proteins in Drosophila are in red, not conserved in blue. Unc is present in Drosophila, not in mammals. (B) Scheme representing centrioles/basal bodies (BBs) at different stages of male germ cells. In early spermatocytes, the two pairs of centrioles (magenta) start to accumulate TZ components (green) at their tips. During spermatocyte maturation, centrioles convert to BBs (magenta), dock to the plasma membrane, and extend cilia/TZ (green). During meiosis, BBs and cilia/TZ are internalized, keeping the ciliary cap connected to the plasma membrane. In round spermatids, the BBs are apposed to the nuclei and extend the ciliary cap (green) connected to the plasma membrane. Ring centriole (blue) connects the base of the ciliary cap to the centriole. Starting axoneme elongation, the ciliary cap is extended, the axoneme grows (black), and the ciliary cap and ring centriole progressively migrate away from the BB.
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fig1: TZ components in Drosophila and scheme of spermatogenesis. (A) Scheme of TZ components present in mammals assigned in different functional modules. Conserved proteins in Drosophila are in red, not conserved in blue. Unc is present in Drosophila, not in mammals. (B) Scheme representing centrioles/basal bodies (BBs) at different stages of male germ cells. In early spermatocytes, the two pairs of centrioles (magenta) start to accumulate TZ components (green) at their tips. During spermatocyte maturation, centrioles convert to BBs (magenta), dock to the plasma membrane, and extend cilia/TZ (green). During meiosis, BBs and cilia/TZ are internalized, keeping the ciliary cap connected to the plasma membrane. In round spermatids, the BBs are apposed to the nuclei and extend the ciliary cap (green) connected to the plasma membrane. Ring centriole (blue) connects the base of the ciliary cap to the centriole. Starting axoneme elongation, the ciliary cap is extended, the axoneme grows (black), and the ciliary cap and ring centriole progressively migrate away from the BB.

Mentions: In mammals and C. elegans, three protein complexes (MKS, NPHP, and CEP290) have been shown to be key players of TZ assembly. CEP290 and most MKS module proteins are conserved in Drosophila, whereas most NPHP components are missing (Fig. 1 A). In addition, Cby and Dila, two proteins conserved in mammals, were shown to be located at the TZ and involved in cilia assembly in Drosophila (Ma and Jarman, 2011; Enjolras et al., 2012). To understand more precisely how these components work together, we tagged several MKS proteins and compared their distribution in relation to Cby and Dila. We previously showed that B9d1 colocalizes with Cby in embryonic sensory cilia (Enjolras et al., 2012). Here, we show that the other members of the MKS module, B9d2, Mks1/B9d3, Tectonic (Tctn), and Cc2d2a, are found at the TZ at the base of sensory cilia as illustrated in chordotonal neurons of the antennae (Fig. S1).


Transition zone assembly and its contribution to axoneme formation in Drosophila male germ cells
TZ components in Drosophila and scheme of spermatogenesis. (A) Scheme of TZ components present in mammals assigned in different functional modules. Conserved proteins in Drosophila are in red, not conserved in blue. Unc is present in Drosophila, not in mammals. (B) Scheme representing centrioles/basal bodies (BBs) at different stages of male germ cells. In early spermatocytes, the two pairs of centrioles (magenta) start to accumulate TZ components (green) at their tips. During spermatocyte maturation, centrioles convert to BBs (magenta), dock to the plasma membrane, and extend cilia/TZ (green). During meiosis, BBs and cilia/TZ are internalized, keeping the ciliary cap connected to the plasma membrane. In round spermatids, the BBs are apposed to the nuclei and extend the ciliary cap (green) connected to the plasma membrane. Ring centriole (blue) connects the base of the ciliary cap to the centriole. Starting axoneme elongation, the ciliary cap is extended, the axoneme grows (black), and the ciliary cap and ring centriole progressively migrate away from the BB.
© Copyright Policy - openaccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5037411&req=5

fig1: TZ components in Drosophila and scheme of spermatogenesis. (A) Scheme of TZ components present in mammals assigned in different functional modules. Conserved proteins in Drosophila are in red, not conserved in blue. Unc is present in Drosophila, not in mammals. (B) Scheme representing centrioles/basal bodies (BBs) at different stages of male germ cells. In early spermatocytes, the two pairs of centrioles (magenta) start to accumulate TZ components (green) at their tips. During spermatocyte maturation, centrioles convert to BBs (magenta), dock to the plasma membrane, and extend cilia/TZ (green). During meiosis, BBs and cilia/TZ are internalized, keeping the ciliary cap connected to the plasma membrane. In round spermatids, the BBs are apposed to the nuclei and extend the ciliary cap (green) connected to the plasma membrane. Ring centriole (blue) connects the base of the ciliary cap to the centriole. Starting axoneme elongation, the ciliary cap is extended, the axoneme grows (black), and the ciliary cap and ring centriole progressively migrate away from the BB.
Mentions: In mammals and C. elegans, three protein complexes (MKS, NPHP, and CEP290) have been shown to be key players of TZ assembly. CEP290 and most MKS module proteins are conserved in Drosophila, whereas most NPHP components are missing (Fig. 1 A). In addition, Cby and Dila, two proteins conserved in mammals, were shown to be located at the TZ and involved in cilia assembly in Drosophila (Ma and Jarman, 2011; Enjolras et al., 2012). To understand more precisely how these components work together, we tagged several MKS proteins and compared their distribution in relation to Cby and Dila. We previously showed that B9d1 colocalizes with Cby in embryonic sensory cilia (Enjolras et al., 2012). Here, we show that the other members of the MKS module, B9d2, Mks1/B9d3, Tectonic (Tctn), and Cc2d2a, are found at the TZ at the base of sensory cilia as illustrated in chordotonal neurons of the antennae (Fig. S1).

View Article: PubMed Central - HTML - PubMed

ABSTRACT

Ciliary transition zone (TZ) assembly is complex and incompletely understood. Vieillard et al. show that Drosophila Cby and Dila cooperate to assemble the TZ and membrane cap, which, together with microtubule remodeling by kinesin-13, is required for axoneme formation in male germ cells.

No MeSH data available.