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Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages


During development, different cell fates are generated by cell–cell interactions or by the asymmetric distribution of patterning molecules. Asymmetric inheritance is known to occur either through directed transport along actin microfilaments into one daughter cell1,2 or through capture of determinants by a region of the cortex inherited by one daughter3,4,5. Here we report a third mechanism of asymmetric inheritance in a mollusc embryo. Different messenger RNAs associate with centrosomes in different cells and are subsequently distributed asymmetrically during division. The segregated mRNAs are diffusely distributed in the cytoplasm and then localize, in a microtubule-dependent manner, to the pericentriolar matrix. During division, they dissociate from the core mitotic centrosome and move by means of actin filaments to the presumptive animal daughter cell cortex. In experimental cells with two interphase centrosomes, mRNAs accumulate on the correct centrosome, indicating that differences between centrosomes control mRNA targeting. Blocking the accumulation of mRNAs on the centrosome shows that this event is required for subsequent cortical localization. These events produce a complex pattern of mRNA localization, in which different messages distinguish groups of cells with the same birth order rank and similar developmental potentials.

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We thank J. Cooley, D. Bentley and J. Wandelt for technical help; J. Salisbury and G. Hermann for antibodies; D. Brower, C. Gregorio and G. Von Dassow for critically reading the manuscript; and R. Palazzo, M. Goulding, G. Lambert, E. Wilk and M. Gibson for technical advice and discussions. This work was supported by an National Science Foundation (NSF) Graduate Research Fellowship and an NSF Doctoral Dissertation Improvement Grant to J.D.L., and a grant from the NSF to L.M.N.

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Correspondence to Lisa M. Nagy.

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Figure 1: Diagram of Ilyanassa cleavage and patterns of centrosomally localized mRNA.
Figure 2: Localization of mRNAs to the centrosome and mRNA dynamics during cleavage.
Figure 3: Cytoskeletal basis of mRNA localization.
Figure 4: mRNAs are localized to specific subsets of cells during cleavage, and mRNAs are specifically targeted to particular centrosomes.


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