Literature DB >> 31443907

Mouth Function Determines the Shape Oscillation Pattern in Regenerating Hydra Tissue Spheres.

Rui Wang1, Tapan Goel2, Kate Khazoyan3, Ziad Sabry4, Heng J Quan5, Patrick H Diamond6, Eva-Maria S Collins7.   

Abstract

Hydra is a small freshwater polyp capable of regeneration from small tissue pieces and from aggregates of cells. During regeneration, a hollow bilayered sphere is formed that undergoes osmotically driven shape oscillations of inflation and rupture. These oscillations are necessary for successful regeneration. Eventually, the oscillating sphere breaks rotational symmetry along the future head-foot axis of the animal. Notably, the shape oscillations show an abrupt shift from large-amplitude, long-period oscillations to small-amplitude, short-period oscillations. It has been widely accepted that this shift in oscillation pattern is linked to symmetry breaking and axis formation, and current theoretical models of Hydra symmetry breaking use this assumption as a model constraint. However, a mechanistic explanation for the shift in oscillation pattern is lacking. Using in vivo manipulation and imaging, we quantified the shape oscillation dynamics and dissected the timing and triggers of the pattern shift. Our experiments demonstrate that the shift in the shape oscillation pattern in regenerating Hydra tissue pieces is caused by the formation of a functional mouth and not by shape symmetry breaking as previously assumed. Thus, model assumptions must be revised in light of these new experimental data, which can be used to constrain and validate improved theoretical models of pattern formation in Hydra.
Copyright © 2019 Biophysical Society. Published by Elsevier Inc. All rights reserved.

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Year:  2019        PMID: 31443907      PMCID: PMC6818176          DOI: 10.1016/j.bpj.2019.07.051

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   4.033


  36 in total

1.  Three digestive movements in Hydra regulated by the diffuse nerve net in the body column.

Authors:  Hiroshi Shimizu; Osamu Koizumi; Toshitaka Fujisawa
Journal:  J Comp Physiol A Neuroethol Sens Neural Behav Physiol       Date:  2004-05-28       Impact factor: 1.836

2.  Head regeneration in wild-type hydra requires de novo neurogenesis.

Authors:  Marijana Miljkovic-Licina; Simona Chera; Luiza Ghila; Brigitte Galliot
Journal:  Development       Date:  2007-02-14       Impact factor: 6.868

3.  Hydra molecular network reaches criticality at the symmetry-breaking axis-defining moment.

Authors:  Jordi Soriano; Cyril Colombo; Albrecht Ott
Journal:  Phys Rev Lett       Date:  2006-12-18       Impact factor: 9.161

Review 4.  Mechanotransduction in development.

Authors:  Emmanuel Farge
Journal:  Curr Top Dev Biol       Date:  2011       Impact factor: 4.897

5.  Generation and Long-term Maintenance of Nerve-free Hydra.

Authors:  Cassidy M Tran; Sharon Fu; Trevor Rowe; Eva-Maria S Collins
Journal:  J Vis Exp       Date:  2017-07-07       Impact factor: 1.355

6.  Preface: the hydra model system.

Authors:  Brigitte Galliot
Journal:  Int J Dev Biol       Date:  2012       Impact factor: 2.203

7.  Generation of transgenic Hydra by embryo microinjection.

Authors:  Celina E Juliano; Haifan Lin; Robert E Steele
Journal:  J Vis Exp       Date:  2014-09-11       Impact factor: 1.355

8.  A theory of biological pattern formation.

Authors:  A Gierer; H Meinhardt
Journal:  Kybernetik       Date:  1972-12

9.  Minimum tissue size required for hydra regeneration.

Authors:  H Shimizu; Y Sawada; T Sugiyama
Journal:  Dev Biol       Date:  1993-02       Impact factor: 3.582

10.  Genetic analysis of developmental mechanisms in Hydra. II. Isolation and characterization of an interstitial cell-deficient strain.

Authors:  T Sugiyama; T Fujisawa
Journal:  J Cell Sci       Date:  1978-02       Impact factor: 5.285

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  1 in total

1.  Mechanical oscillations orchestrate axial patterning through Wnt activation in Hydra.

Authors:  Jaroslav Ferenc; Panagiotis Papasaikas; Jacqueline Ferralli; Yukio Nakamura; Sebastien Smallwood; Charisios D Tsiairis
Journal:  Sci Adv       Date:  2021-12-10       Impact factor: 14.136

  1 in total

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