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Meiotic prophase-like pathway for cleavage-independent removal of cohesin for chromosome morphogenesis

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Abstract

Sister chromatid cohesion is essential for chromosome segregation both in mitosis and meiosis. Cohesion between two chromatids is mediated by a protein complex called cohesin. The loading and unloading of the cohesin are tightly regulated during the cell cycle. In vertebrate cells, cohesin is released from chromosomes by two distinct pathways. The best characterized pathway occurs at the onset of anaphase, when the kleisin component of the cohesin is destroyed by a protease, separase. The cleavage of the cohesin by separase releases entrapped sister chromatids allowing anaphase to commence. In addition, prior to the metaphase–anaphase transition, most of cohesin is removed from chromosomes in a cleavage-independent manner. This cohesin release is referred to as the prophase pathway. In meiotic cells, sister chromatid cohesion is essential for the segregation of homologous chromosomes during meiosis I. Thus, it was assumed that the prophase pathway for cohesin removal from chromosome arms would be suppressed during meiosis to avoid errors in chromosome segregation. However, recent studies revealed the presence of a meiosis-specific prophase-like pathway for cleavage-independent removal of cohesin during late prophase I in different organisms. In budding yeast, the cleavage-independent removal of cohesin is mediated through meiosis-specific phosphorylation of cohesin subunits, Rec8, the meiosis-specific kleisin, and the yeast Wapl ortholog, Rad61/Wpl1. This pathway plays a role in chromosome morphogenesis during late prophase I, promoting chromosome compaction. In this review, we give an overview of the prophase pathway for cohesin dynamics during meiosis, which has a complex regulation leading to differentially localized populations of cohesin along meiotic chromosomes.

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Acknowledgements

We are grateful for Drs. Susan Gasser and Franz Klein for constructive comments on the paper. We also thank Dr. K. Kim for strains. This work was supported by JSPS KAKENHI Grant Numbers; 22125001, 22125002, 15H05973 and 16H04742 to A.S.

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KC and AS wrote an initial draft and AS revised. KC, MS, and AS edited the manuscript.

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Correspondence to Akira Shinohara.

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Communicated by M. Kupiec.

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Challa, K., Shinohara, M. & Shinohara, A. Meiotic prophase-like pathway for cleavage-independent removal of cohesin for chromosome morphogenesis. Curr Genet 65, 817–827 (2019). https://doi.org/10.1007/s00294-019-00959-x

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  • DOI: https://doi.org/10.1007/s00294-019-00959-x

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