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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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Model of PLP-Cnn coregulation at interphase centrosomes. Diagram depicting centrosome scaffold formation during interphase. Our data support an interphase-specific Cnn scaffold in the interphase flare zone that is organized by PLP satellites. See text for details.
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fig10: Model of PLP-Cnn coregulation at interphase centrosomes. Diagram depicting centrosome scaffold formation during interphase. Our data support an interphase-specific Cnn scaffold in the interphase flare zone that is organized by PLP satellites. See text for details.

Mentions: SIM confirms that interphase centrosomes in cnnB4 embryos lack PLP satellites but maintain PLP at centrioles (Fig. 9 B), which signifies that the two PLP pools are regulated by distinct mechanisms. Furthermore, we conclude that the Cnn(CM2)–PLP(F2) interaction is dispensable for PLP centriole localization but is essential for PLP satellite formation. The lack of PLP satellites in cnnB4 embryos corresponds with a loss of Cnn flares and an increase in Cnn cytoplasmic particles, similar to the plp− phenotype (Figs. 5 F and 9 B). While it remains formally possible that the cnnB4 mutation abrogates the structure of the Cnn molecule and/or its overall function, mitotic cnnB4 centrosomes are much less disrupted (Kao and Megraw, 2009), suggesting that the pathway that organizes Cnn during mitosis remains intact and that the Cnn molecule is not completely disrupted. Therefore, we propose that PLP satellites function to form a Cnn scaffold in the interphase flare zone that organizes and confines Cnn to interphase centrosomes (Fig. 10). Our data demonstrate that Cnn and PLP are mutually required for the proper localization and function of the other, thereby demonstrating the presence of a positive feedback loop that ensures the proper formation of the interphase centrosome scaffold.


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)

Model of PLP-Cnn coregulation at interphase centrosomes. Diagram depicting centrosome scaffold formation during interphase. Our data support an interphase-specific Cnn scaffold in the interphase flare zone that is organized by PLP satellites. See text for details.
© Copyright Policy - openaccess
Related In: Results  -  Collection

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

fig10: Model of PLP-Cnn coregulation at interphase centrosomes. Diagram depicting centrosome scaffold formation during interphase. Our data support an interphase-specific Cnn scaffold in the interphase flare zone that is organized by PLP satellites. See text for details.
Mentions: SIM confirms that interphase centrosomes in cnnB4 embryos lack PLP satellites but maintain PLP at centrioles (Fig. 9 B), which signifies that the two PLP pools are regulated by distinct mechanisms. Furthermore, we conclude that the Cnn(CM2)–PLP(F2) interaction is dispensable for PLP centriole localization but is essential for PLP satellite formation. The lack of PLP satellites in cnnB4 embryos corresponds with a loss of Cnn flares and an increase in Cnn cytoplasmic particles, similar to the plp− phenotype (Figs. 5 F and 9 B). While it remains formally possible that the cnnB4 mutation abrogates the structure of the Cnn molecule and/or its overall function, mitotic cnnB4 centrosomes are much less disrupted (Kao and Megraw, 2009), suggesting that the pathway that organizes Cnn during mitosis remains intact and that the Cnn molecule is not completely disrupted. Therefore, we propose that PLP satellites function to form a Cnn scaffold in the interphase flare zone that organizes and confines Cnn to interphase centrosomes (Fig. 10). Our data demonstrate that Cnn and PLP are mutually required for the proper localization and function of the other, thereby demonstrating the presence of a positive feedback loop that ensures the proper formation of the interphase centrosome scaffold.

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