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A selective block of nuclear actin export stabilizes the giant nuclei of Xenopus oocytes

Abstract

Actin is a major cytoskeletal element and is normally kept cytoplasmic by exportin 6 (Exp6)-driven nuclear export. Here, we show that Exp6 recognizes actin features that are conserved from yeast to human. Surprisingly however, microinjected actin was not exported from Xenopus laevis oocyte nuclei, unless Exp6 was co-injected, indicating that the pathway is inactive in this cell type. Indeed, Exp6 is undetectable in oocytes, but is synthesized from meiotic maturation onwards, which explains how actin export resumes later in embryogenesis. Exp6 thus represents the first example of a strictly developmentally regulated nuclear transport pathway. We asked why Xenopus oocytes lack Exp6 and observed that ectopic application of Exp6 renders the giant oocyte nuclei extremely fragile. This effect correlates with the selective disappearance of a sponge-like intranuclear scaffold of F-actin. These nuclei have a normal G2-phase DNA content in a volume 100,000 times larger than nuclei of somatic cells. Apparently, their mechanical integrity cannot be maintained by chromatin and the associated nuclear matrix, but instead requires an intranuclear actin-scaffold.

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Figure 1: Actin export from nuclei of Xenopus oocytes requires exogenous Exp6.
Figure 2: Xenopus Exp6 is active in nuclear actin export.
Figure 3: Xenopus oocytes stockpile Exp6 mRNA, but selectively lack the Exp6 protein.
Figure 4: Synthesis of the Exp6 protein is induced during meiotic maturation.
Figure 5: Exp6 depletes the large actin pool from nuclei of Xenopus ooctyes.
Figure 6: A sponge-like actin meshwork within nuclei of Xenopus oocytes.

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Acknowledgements

We wish to thank P. Rübmann, U. Jäkle and the animal facility of the ZMBH for excellent technical help, and J. Gall as well as the members of our laboratory for very helpful comments on the manuscript. This work received financial support from the Deutsche Forschungsgemeinschaft (SFB 638) and the Alfried–Krupp Foundation.

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Correspondence to Dirk Görlich.

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Bohnsack, M., Stüven, T., Kuhn, C. et al. A selective block of nuclear actin export stabilizes the giant nuclei of Xenopus oocytes. Nat Cell Biol 8, 257–263 (2006). https://doi.org/10.1038/ncb1357

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