Ingression Progression Complexes Control Extracellular Matrix Remodelling during Cytokinesis in Budding Yeast.

Magdalena Foltman,Irene Arcones,Alberto Sanchez-Diaz,Yasmina Filali-Mouncef,Carlos Sacristan,Cesar Roncero,Iago Molist,Kathleen L Gould

doi:10.1371/journal.pgen.1005864

Abstract

Eukaryotic cells must coordinate contraction of the actomyosin ring at the division site together with ingression of the plasma membrane and remodelling of the extracellular matrix (ECM) to support cytokinesis, but the underlying mechanisms are still poorly understood. In eukaryotes, glycosyltransferases that synthesise ECM polysaccharides are emerging as key factors during cytokinesis. The budding yeast chitin synthase Chs2 makes the primary septum, a special layer of the ECM, which is an essential process during cell division. Here we isolated a group of actomyosin ring components that form complexes together with Chs2 at the cleavage site at the end of the cell cycle, which we named ‘ingression progression complexes’ (IPCs). In addition to type II myosin, the IQGAP protein Iqg1 and Chs2, IPCs contain the F-BAR protein Hof1, and the cytokinesis regulators Inn1 and Cyk3. We describe the molecular mechanism by which chitin synthase is activated by direct association of the C2 domain of Inn1, and the transglutaminase-like domain of Cyk3, with the catalytic domain of Chs2. We used an experimental system to find a previously unanticipated role for the C-terminus of Inn1 in preventing the untimely activation of Chs2 at the cleavage site until Cyk3 releases the block on Chs2 activity during late mitosis. These findings support a model for the co-ordinated regulation of cell division in budding yeast, in which IPCs play a central role.

Highlights

Eukaryotic cells divide their cytoplasm at the end of mitosis in a highly regulated process called cytokinesis, which safeguards inheritance of the genome and organelles by the two daughter cells
Contraction of the actomyosin ring is coupled to ingression of the plasma membrane and extracellular matrix remodelling
Glycosyltransferases that synthesise polysaccharides of the extracellular matrix are emerging as essential factors during cytokinesis

Summary

Introduction

Eukaryotic cells divide their cytoplasm at the end of mitosis in a highly regulated process called cytokinesis, which safeguards inheritance of the genome and organelles by the two daughter cells. The ECM is composed of a collection of biochemically distinct components, among which polysaccharides are emerging as key factors during cytokinesis, as shown by the failure in cytokinesis caused by defects associated with their synthesis in evolutionary distant organisms such as the budding yeast Saccharomyces cerevisiae [7] [8], the fission yeast Schizosaccharomyces pombe [9] [10] [11], the nematode Caenorhabditis elegans [12] and the mouse [13] In these four examples, the impairment of a glycosyltransferase determines clear cell division defects. Chitin is a polymer of N-acetylglucosamine (Glc-NAc), which is synthesised from an activated nucleotide substrate UDP-N-acetylglucosamine (UDP-GlcNAc), and chitin chains are subsequently secreted outside the cells, assembled into microfibrils and organised in the extracellular matrix [14] [15]

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