Literature DB >> 25047608

Organization of early frog embryos by chemical waves emanating from centrosomes.

Keisuke Ishihara1, Phuong A Nguyen2, Martin Wühr2, Aaron C Groen2, Christine M Field2, Timothy J Mitchison2.   

Abstract

The large cells in early vertebrate development face an extreme physical challenge in organizing their cytoplasm. For example, amphibian embryos have to divide cytoplasm that spans hundreds of micrometres every 30 min according to a precise geometry, a remarkable accomplishment given the extreme difference between molecular and cellular scales in this system. How do the biochemical reactions occurring at the molecular scale lead to this emergent behaviour of the cell as a whole? Based on recent findings, we propose that the centrosome plays a crucial role by initiating two autocatalytic reactions that travel across the large cytoplasm as chemical waves. Waves of mitotic entry and exit propagate out from centrosomes using the Cdk1 oscillator to coordinate the timing of cell division. Waves of microtubule-stimulated microtubule nucleation propagate out to assemble large asters that position spindles for the following mitosis and establish cleavage plane geometry. By initiating these chemical waves, the centrosome rapidly organizes the large cytoplasm during the short embryonic cell cycle, which would be impossible using more conventional mechanisms such as diffusion or nucleation by structural templating. Large embryo cells provide valuable insights to how cells control chemical waves, which may be a general principle for cytoplasmic organization.
© 2014 The Author(s) Published by the Royal Society. All rights reserved.

Entities:  

Keywords:  cell cycle; centrosome; chemical wave; embryo; microtubule aster

Mesh:

Substances:

Year:  2014        PMID: 25047608      PMCID: PMC4113098          DOI: 10.1098/rstb.2013.0454

Source DB:  PubMed          Journal:  Philos Trans R Soc Lond B Biol Sci        ISSN: 0962-8436            Impact factor:   6.237


  74 in total

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Review 2.  Microtubule oscillations.

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Authors:  Takashi Murata; Seiji Sonobe; Tobias I Baskin; Susumu Hyodo; Seiichiro Hasezawa; Toshiyuki Nagata; Tetsuya Horio; Mitsuyasu Hasebe
Journal:  Nat Cell Biol       Date:  2005-09-04       Impact factor: 28.824

4.  Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network.

Authors:  Andrey Efimov; Alexey Kharitonov; Nadia Efimova; Jadranka Loncarek; Paul M Miller; Natalia Andreyeva; Paul Gleeson; Niels Galjart; Ana R R Maia; Ian X McLeod; John R Yates; Helder Maiato; Alexey Khodjakov; Anna Akhmanova; Irina Kaverina
Journal:  Dev Cell       Date:  2007-06       Impact factor: 12.270

5.  Protein mobility in the cytoplasm of Escherichia coli.

Authors:  M B Elowitz; M G Surette; P E Wolf; J B Stock; S Leibler
Journal:  J Bacteriol       Date:  1999-01       Impact factor: 3.490

6.  Microtubule minus-end stabilization by polymerization-driven CAMSAP deposition.

Authors:  Kai Jiang; Shasha Hua; Renu Mohan; Ilya Grigoriev; Kah Wai Yau; Qingyang Liu; Eugene A Katrukha; A F Maarten Altelaar; Albert J R Heck; Casper C Hoogenraad; Anna Akhmanova
Journal:  Dev Cell       Date:  2014-01-30       Impact factor: 12.270

7.  A cytoplasmic clock with the same period as the division cycle in Xenopus eggs.

Authors:  K Hara; P Tydeman; M Kirschner
Journal:  Proc Natl Acad Sci U S A       Date:  1980-01       Impact factor: 11.205

8.  Evidence for an upper limit to mitotic spindle length.

Authors:  Martin Wühr; Yao Chen; Sophie Dumont; Aaron C Groen; Daniel J Needleman; Adrian Salic; Timothy J Mitchison
Journal:  Curr Biol       Date:  2008-08-26       Impact factor: 10.834

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Authors:  F Verde; M Dogterom; E Stelzer; E Karsenti; S Leibler
Journal:  J Cell Biol       Date:  1992-09       Impact factor: 10.539

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Authors:  Orion D Weiner; William A Marganski; Lani F Wu; Steven J Altschuler; Marc W Kirschner
Journal:  PLoS Biol       Date:  2007-09       Impact factor: 8.029

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  14 in total

1.  Microtubule nucleation remote from centrosomes may explain how asters span large cells.

Authors:  Keisuke Ishihara; Phuong A Nguyen; Aaron C Groen; Christine M Field; Timothy J Mitchison
Journal:  Proc Natl Acad Sci U S A       Date:  2014-12-02       Impact factor: 11.205

2.  Centrosomes back in the limelight.

Authors:  Michel Bornens; Pierre Gönczy
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2014-09-05       Impact factor: 6.237

Review 3.  Organelle size scaling over embryonic development.

Authors:  Chase C Wesley; Sampada Mishra; Daniel L Levy
Journal:  Wiley Interdiscip Rev Dev Biol       Date:  2020-01-31       Impact factor: 5.814

4.  Proteomics of phosphorylation and protein dynamics during fertilization and meiotic exit in the Xenopus egg.

Authors:  Marc Presler; Elizabeth Van Itallie; Allon M Klein; Ryan Kunz; Margaret L Coughlin; Leonid Peshkin; Steven P Gygi; Martin Wühr; Marc W Kirschner
Journal:  Proc Natl Acad Sci U S A       Date:  2017-11-28       Impact factor: 11.205

5.  Nuclei determine the spatial origin of mitotic waves.

Authors:  Felix E Nolet; Alexandra Vandervelde; Arno Vanderbeke; Liliana Piñeros; Jeremy B Chang; Lendert Gelens
Journal:  Elife       Date:  2020-05-26       Impact factor: 8.140

6.  Waves of Cdk1 Activity in S Phase Synchronize the Cell Cycle in Drosophila Embryos.

Authors:  Victoria E Deneke; Anna Melbinger; Massimo Vergassola; Stefano Di Talia
Journal:  Dev Cell       Date:  2016-08-22       Impact factor: 12.270

7.  Physical basis of large microtubule aster growth.

Authors:  Keisuke Ishihara; Kirill S Korolev; Timothy J Mitchison
Journal:  Elife       Date:  2016-11-28       Impact factor: 8.140

Review 8.  Chemical waves in cell and developmental biology.

Authors:  Victoria E Deneke; Stefano Di Talia
Journal:  J Cell Biol       Date:  2018-01-09       Impact factor: 10.539

9.  Autocatalytic microtubule nucleation determines the size and mass of Xenopus laevis egg extract spindles.

Authors:  Franziska Decker; David Oriola; Benjamin Dalton; Jan Brugués
Journal:  Elife       Date:  2018-01-11       Impact factor: 8.140

Review 10.  Rhythmicity and waves in the cortex of single cells.

Authors:  Yang Yang; Min Wu
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2018-05-26       Impact factor: 6.237

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