Editors' ChoiceCell Cycle

Autonomous Cycling in a Shared Cytoplasm

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Science Signaling  09 Jul 2013:
Vol. 6, Issue 283, pp. ec155
DOI: 10.1126/scisignal.2004487

In the multinucleate filamentous fungus Ashbya gossypii, nuclei divide asynchronously despite sharing a common cytoplasm. Using single-molecule fluorescence in situ hybridization, Lee et al. report that mRNAs encoding the G1 cyclin CLN3, which controls the G1 to S transition, were asymmetrically clustered in the cytoplasm of Ashbya cells. CLN3 transcripts contain binding sites for the RNA-binding protein Whi3, and CLN3 transcripts were bound to Whi3 immunoprecipitated from lysates of Ashbya cells expressing a tagged version of Whi3. In vitro binding assays using bacterially expressed, tagged Whi3 and mRNAs isolated from Ashbya cell lysates suggested that the interaction was direct. CLN3 transcripts were randomly distributed in whi3-null cells and in cells carrying a mutant version of Whi3 lacking its C-terminal RNA-recognition motif (RRM). Whi3 was distributed in puncta in the cytoplasm of Ashbya cells, and a polyglutamine tract in the middle of Whi3 was required for this nonrandom distribution. Cells expressing Whi3 that had the polyglutamine tract replaced with a nonrepetitive sequence also showed a random distribution of CLN3 transcripts. Whereas nuclei divided asynchronously in wild-type cells, nuclear divisions were synchronous in whi3-null cells. Whi3 diffused slowly in cells, suggesting that it was part of a larger complex, leading the authors to propose that the polyglutamine tract of Whi3 mediates prion-like aggregation of Whi3-CLN3 complexes. Associated commentary by Alberti considers other possible mechanisms for Whi3-CLN3 clustering. There are many examples of the establishment and function of subcellularly localized transcripts in embryos and polarized cells, and this study implies that localized mRNAs may also control regional processes in nonpolarized cells.

C. Lee, H. Zhang, A. E. Baker, P. Occhipinti, M. E. Borsuk, A. S. Gladfelter, Protein aggregation behavior regulates cyclin transcript localization and cell-cycle control. Dev. Cell 25, 572–584 (2013). [PubMed]

S. Alberti, Aggregating the message to control the cell cycle. Dev. Cell 25, 551–552 (2013). [PubMed]

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