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A journey into space

Nature Reviews Molecular Cell Biology volume 2, pages 647–656 (2001)Cite this article

Key Points

  • Microtubules are important components for establishing positional information, and are required to establish a cellular axis and to position the nucleus.

  • Several proteins have been identified that are required to establish an axis. In the absence of these proteins, fission yeast cells no longer grow in a straight line. These proteins include Tea1, Tea2, Tip1, Mal3, γ-tubulin, Alp4 and Alp6, all of which affect microtubule dynamics, and several proteins required for microtubule biogenesis.

  • Many of the proteins identified in fission yeast are also conserved in other organisms. The CLIP170 protein family regulates microtubule dynamics and might be involved in a microtubule guidance mechanism, both in fission yeast and other eukaryotes.

  • Three models have been proposed that might guide microtubules along an axis and identify the ends of the cell. One of these models depends on the presence of historical markers; one depends more on the self organization of microtubules, together with marker proteins that can act as catastrophe factors; and the third depends on the ability of microtubules to withstand pressure. These models are not mutually exclusive.

  • The nucleus might be positioned at the cell centre by a balance of pushing forces generated by interphase microtubules. A second mechanism that positions the daughter nuclei at the cell centre after mitosis might depend on a pulling mechanism so that the nucleus is pulled to the cell centre by the post-anaphase array of microtubules. Microtubules and motor proteins are also required to position the nucleus in other organisms.

  • Similar microtubular behaviour might be the basis of mechanisms to define the long axis of the cell and to position the nucleus at the cell centre.

Abstract

The fission yeast, Schizosaccharomyces pombe, has been used as a model eukaryote to study processes such as the cell cycle and cell morphology. In this single-celled organism, growing in a straight line and maintaining the nucleus in the centre of the cell depend on intracellular positional information. Microtubules and microtubular transport are important for generating positional information within the fission yeast cell, and these molecular mechanisms are also probably relevant for generating positional information in other eukaryotic cells.

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Figure 1: Growth and cytoskeletal changes during the cell cycle.
Figure 2: Microtubules in wild-type cells.
Figure 3: Morphology mutants of fission yeast.
Figure 4: Microtubules in cells lacking tea-interacting protein 1.
Figure 5: Photographs of fixed cells.
Figure 6: Models of how microtubules align along the long axis of the cell and stop growth at the ends of the cell.

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Acknowledgements

We would like to thank everyone in the cell-cycle lab at ICRF, particularly Heidi Browning and Teresa Niccoli for their useful comments. We are also very grateful to Bela Novak, Bela Gyoffy, Attila Csikasz-Nagy and Akos Sveiczer at the Budapest University of Technology and Economics for fruitful discussions at the workshop on morphology held in Budapest, May 2000.

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Authors and Affiliations

  1. Cell Cycle Laboratory, Imperial Cancer Research Fund, PO Box 123, Lincoln's Inn Fields, London, WC2A 3PX, UK

    Jacqueline Hayles & Paul Nurse

  2. Jacqueline Hayles

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  1. Jacqueline Hayles
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DATABASE LINKS

tea1

mal3

EB1

APC

familial adenomatous polyposis coli

gtb1

alp4

alp6

Glossary

MICROTUBULE-ORGANIZING CENTRE

A γ-tubulin-containing region from which microtubules are polymerized.

CATASTROPHE

Rapid shrinkage of microtubules from their plus ends, due to loss of α/β-subunits.

KELCH REPEATS

A domain covering repeats of ∼50 amino acids containing conserved residues, which folds into a β-propeller secondary structure, first identified in kelch proteins and found in several actin-binding proteins.

COILED-COIL

A region of protein secondary structure that might be involved in protein–protein interactions.

KINESIN MOTOR DOMAIN

A conserved region of ∼350 amino acids, defining members of the kinesin superfamily and required for ATP-dependent translocation along microtubules.

CLIP170 PROTEIN FAMILY

Proteins found at the tips of microtubules and involved in microtubule stability; initially described as linking microtubules to vesicles.

CENTROSOMES

The microtubule-organizing centres in higher eukaryotes; associated with the mitotic spindle and astral microtubules and from which microtubules radiate during interphase.

DESMOSOMAL PLAQUES

Regions of anchorage linking adjacent cells and containing intracellular attachment proteins and transmembrane linker glycoproteins.

PRONUCLEUS

The nucleus from an egg or sperm that contains a single copy of each chromosome pair.

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Hayles, J., Nurse, P. A journey into space. Nat Rev Mol Cell Biol 2, 647–656 (2001). https://doi.org/10.1038/35089520

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