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Interphase centrosome organization by the PLP-Cnn scaffold is required for centrosome function.

Lerit DA, Jordan HA, Poulton JS, Fagerstrom CJ, Galletta BJ, Peifer M, Rusan NM - J. Cell Biol. (2015)

Bottom Line: Pericentriolar material (PCM) mediates the microtubule (MT) nucleation and anchoring activity of centrosomes.A scaffold organized by Centrosomin (Cnn) serves to ensure proper PCM architecture and functional changes in centrosome activity with each cell cycle.Focusing on the mitotic-to-interphase transition in Drosophila melanogaster embryos, we show that the elaboration of the interphase Cnn scaffold defines a major structural rearrangement of the centrosome.

View Article: PubMed Central - HTML - PubMed

Affiliation: Cell Biology and Physiology Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892.

ABSTRACT
Pericentriolar material (PCM) mediates the microtubule (MT) nucleation and anchoring activity of centrosomes. A scaffold organized by Centrosomin (Cnn) serves to ensure proper PCM architecture and functional changes in centrosome activity with each cell cycle. Here, we investigate the mechanisms that spatially restrict and temporally coordinate centrosome scaffold formation. Focusing on the mitotic-to-interphase transition in Drosophila melanogaster embryos, we show that the elaboration of the interphase Cnn scaffold defines a major structural rearrangement of the centrosome. We identify an unprecedented role for Pericentrin-like protein (PLP), which localizes to the tips of extended Cnn flares, to maintain robust interphase centrosome activity and promote the formation of interphase MT asters required for normal nuclear spacing, centrosome segregation, and compartmentalization of the syncytial embryo. Our data reveal that Cnn and PLP directly interact at two defined sites to coordinate the cell cycle-dependent rearrangement and scaffolding activity of the centrosome to permit normal centrosome organization, cell division, and embryonic viability.

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Cnn and PLP are packaged together into dynamic flares. (A) Live PLPFL and Cnn-mCherry at two centrosome pairs within a single embryo show coincidence (arrowheads) at the tip of an extended flare. Red arrows show particle release. (B) Particle associates with existing PCM (green arrows). The asterisks mark the centriole. Time is given in seconds. Bars, 1 µm.
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fig4: Cnn and PLP are packaged together into dynamic flares. (A) Live PLPFL and Cnn-mCherry at two centrosome pairs within a single embryo show coincidence (arrowheads) at the tip of an extended flare. Red arrows show particle release. (B) Particle associates with existing PCM (green arrows). The asterisks mark the centriole. Time is given in seconds. Bars, 1 µm.

Mentions: In contrast, we find endogenous PLP at high levels in nearly every Cnn flare (94.7%; n = 190 flares, 82 centrosomes) in addition to its known centriole localization, which suggests that PLP may coordinate centrosome shape changes with Cnn, while almost no PLP is detected in the PCM zone (Figs. 2, B–D′). More than two decades ago, Pcnt was localized to “PCM-like bodies (satellites)” in mammalian cells using immuno-EM (see Fig. 4; Doxsey et al., 1994). Subsequent work proved that Pcnt forms a biochemical complex with the canonical mammalian centriole satellite marker, PCM-1 (Li et al., 2001; Dammermann and Merdes, 2002). Although a functional orthologue of PCM-1 has not been identified in Drosophila, the discrete localization of PLP foci at flare tips is reminiscent of satellites orbiting a central body (the centriole); therefore, we refer to PLP localized within the interphase flare zone as PLP satellites.


Interphase centrosome organization by the PLP-Cnn scaffold is required for centrosome function.

Lerit DA, Jordan HA, Poulton JS, Fagerstrom CJ, Galletta BJ, Peifer M, Rusan NM - J. Cell Biol. (2015)

Cnn and PLP are packaged together into dynamic flares. (A) Live PLPFL and Cnn-mCherry at two centrosome pairs within a single embryo show coincidence (arrowheads) at the tip of an extended flare. Red arrows show particle release. (B) Particle associates with existing PCM (green arrows). The asterisks mark the centriole. Time is given in seconds. Bars, 1 µm.
© Copyright Policy - openaccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4494003&req=5

fig4: Cnn and PLP are packaged together into dynamic flares. (A) Live PLPFL and Cnn-mCherry at two centrosome pairs within a single embryo show coincidence (arrowheads) at the tip of an extended flare. Red arrows show particle release. (B) Particle associates with existing PCM (green arrows). The asterisks mark the centriole. Time is given in seconds. Bars, 1 µm.
Mentions: In contrast, we find endogenous PLP at high levels in nearly every Cnn flare (94.7%; n = 190 flares, 82 centrosomes) in addition to its known centriole localization, which suggests that PLP may coordinate centrosome shape changes with Cnn, while almost no PLP is detected in the PCM zone (Figs. 2, B–D′). More than two decades ago, Pcnt was localized to “PCM-like bodies (satellites)” in mammalian cells using immuno-EM (see Fig. 4; Doxsey et al., 1994). Subsequent work proved that Pcnt forms a biochemical complex with the canonical mammalian centriole satellite marker, PCM-1 (Li et al., 2001; Dammermann and Merdes, 2002). Although a functional orthologue of PCM-1 has not been identified in Drosophila, the discrete localization of PLP foci at flare tips is reminiscent of satellites orbiting a central body (the centriole); therefore, we refer to PLP localized within the interphase flare zone as PLP satellites.

Bottom Line: Pericentriolar material (PCM) mediates the microtubule (MT) nucleation and anchoring activity of centrosomes.A scaffold organized by Centrosomin (Cnn) serves to ensure proper PCM architecture and functional changes in centrosome activity with each cell cycle.Focusing on the mitotic-to-interphase transition in Drosophila melanogaster embryos, we show that the elaboration of the interphase Cnn scaffold defines a major structural rearrangement of the centrosome.

View Article: PubMed Central - HTML - PubMed

Affiliation: Cell Biology and Physiology Center, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892.

ABSTRACT
Pericentriolar material (PCM) mediates the microtubule (MT) nucleation and anchoring activity of centrosomes. A scaffold organized by Centrosomin (Cnn) serves to ensure proper PCM architecture and functional changes in centrosome activity with each cell cycle. Here, we investigate the mechanisms that spatially restrict and temporally coordinate centrosome scaffold formation. Focusing on the mitotic-to-interphase transition in Drosophila melanogaster embryos, we show that the elaboration of the interphase Cnn scaffold defines a major structural rearrangement of the centrosome. We identify an unprecedented role for Pericentrin-like protein (PLP), which localizes to the tips of extended Cnn flares, to maintain robust interphase centrosome activity and promote the formation of interphase MT asters required for normal nuclear spacing, centrosome segregation, and compartmentalization of the syncytial embryo. Our data reveal that Cnn and PLP directly interact at two defined sites to coordinate the cell cycle-dependent rearrangement and scaffolding activity of the centrosome to permit normal centrosome organization, cell division, and embryonic viability.

Show MeSH
Related in: MedlinePlus