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Self-organization of interphase microtubule arrays in fission yeast

Nature Cell Biology volume 8, pages 1102–1107 (2006)Cite this article

Abstract

Microtubule organization is key to eukaryotic cell structure and function. In most animal cells, interphase microtubules organize around the centrosome, the major microtubule organizing centre (MTOC). Interphase microtubules can also become organized independently of a centrosome, but how acentrosomal microtubules arrays form and whether they are functionally equivalent to centrosomal arrays remains poorly understood1,2. Here, we show that the interphase microtubule arrays of fission yeast cells can persist independently of nuclear-associated MTOCs, including the spindle pole body (SPB) — the centrosomal equivalent. By artificially enucleating cells, we show that arrays can form de novo (self-organize) without nuclear-associated MTOCs, but require the microtubule nucleator mod20–mbo1–mto1 (refs 3–5), the bundling factor ase1 (refs 6,7), and the kinesin klp2 (refs 8,9). Microtubule arrays in enucleated and nucleated cells are morphologically indistinguishable and similarly locate to the cellular axis and centre. By simultaneously tracking nuclear-independent and SPB-associated microtubule arrays within individual nucleated cells, we show that both define the cell centre with comparable precision. We propose that in fission yeast, nuclear-independent, self-organized, acentrosomal microtubule arrays are structurally and functionally equivalent to centrosomal arrays.

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Figure 1: Nucleus-independent maintenance of interphase microtubule organization.
Figure 2: Self-organization of interphase microtubule arrays in enucleated yeast cells.
Figure 3: Precision in interphase microtubule array self-centring.
Figure 4: Schematic representation of a proposed model for self-organization of interphase microtubule arrays in fission yeast.

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Acknowledgements

We thank E. Piddini, R. Daga, M. Pardo, M. Godinho-Ferreira, B. Novák, T. Surrey, M. Sato, T. Toda, F. Uhlmann and T. Wittmann, and members of the Nurse lab for discussions; O. Niwa, K. Sawin, and T. Toda for materials; and E. Piddini, T. Surrey, M. Godinho-Ferreira, O. Rog, J. Hayles, S. Castagnetti, F. Uhlmann and T. Wittmann for reading the manuscript. R.E.C.S. was supported by International Human Frontier Science Program (HFSP) and Cancer Research UK postdoctoral fellowships and P.N. was supported by Cancer Research UK and the Rockefeller University.

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  1. Cell Cycle Laboratory, 44 Lincoln's Inn Fields, Cancer Research UK, London Research Institute, WC2A 1PX, UK

    Rafael E. Carazo-Salas & Paul Nurse

  2. Laboratory of Yeast Genetics and Cell Biology, Rockefeller University, 1230 York Avenue, New York, 10021, NY, USA

    Paul Nurse

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  1. Rafael E. Carazo-Salas
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Correspondence to Rafael E. Carazo-Salas.

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Carazo-Salas, R., Nurse, P. Self-organization of interphase microtubule arrays in fission yeast. Nat Cell Biol 8, 1102–1107 (2006). https://doi.org/10.1038/ncb1479

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