The role of mesoglea in mass cell movement in Hydra

Shostak, Stanley; Patel, Narayan G.; Burnett, Allison L.

doi:10.1016/0012-1606(65)90008-4

Cited by 83 publications

(33 citation statements)

References 14 publications

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“…Thus, not only epithelial sheets but also the intervening mesoglea is subjected to a constant centrifugal tissue renewal. These observations reject the assumption that the general nature of Hydra tissue movements represents active epithelial migration relative to a stationary mesoglea Shostak and Globus, 1966;Shostak et al, 1965). Rather, they support the view of Campbell (Campbell, 1973;Campbell, 1974) that the apparent 'movement' of epithelial cells relative to the morphology of the animal can be understood as continuous 'outward' expansion of the whole tissue.…”

Section: The Role Of Mesoglea During Hydra Tissue Movementscontrasting

confidence: 43%

“…This does not lead to an increase in body size because, under steady state conditions, tissue growth is balanced by tissue loss at the ends of the body column and in developing buds. These tissue movements have been systematically investigated with the help of various in vivo markers for ectodermal and endodermal epithelial cells (Campbell, 1967b;Campbell, 1973;Otto and Campbell, 1977a;Shostak and Kankel, 1967;Shostak et al, 1965;Wittlieb et al, 2006). However, the role of the mesoglea has remained unclear.…”

Section: Introductionmentioning

confidence: 99%

“…However, the role of the mesoglea has remained unclear. Two opposing views are possible: (1) the mesoglea is a stationary structure that serves as a substratum for active epithelial motility (Shostak and Globus, 1966;Shostak et al, 1965), or (2) tissue movements are the result of continuous tissue expansion that includes both epithelia and the mesoglea (Campbell, 1973;Campbell, 1974).…”

Section: Introductionmentioning

confidence: 99%

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In vivo imaging of basement membrane movement: ECM patterning shapesHydrapolyps

Aufschnaiter

Zamir

Little

et al. 2011

Journal of Cell Science

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SummaryGrowth and morphogenesis during embryonic development, asexual reproduction and regeneration require extensive remodeling of the extracellular matrix (ECM). We used the simple metazoan Hydra to examine the fate of ECM during tissue morphogenesis and asexual budding. In growing Hydra, epithelial cells constantly move towards the extremities of the animal and into outgrowing buds. It is not known, whether these tissue movements involve epithelial migration relative to the underlying matrix or whether cells and ECM are displaced as a composite structure. Furthermore, it is unclear, how the ECM is remodeled to adapt to the shape of developing buds and tentacles. To address these questions, we used a new in vivo labeling technique for Hydra collagen-1 and laminin, and tracked the fate of ECM in all body regions of the animal. Our results reveal that Hydra 'tissue movements' are largely displacements of epithelial cells together with associated ECM. By contrast, during the evagination of buds and tentacles, extensive movement of epithelial cells relative to the matrix is observed, together with local ECM remodeling. These findings provide new insights into the nature of growth and morphogenesis in epithelial tissues.

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Section: The Role Of Mesoglea During Hydra Tissue Movementscontrasting

confidence: 43%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

In vivo imaging of basement membrane movement: ECM patterning shapesHydrapolyps

Aufschnaiter

Zamir

Little

et al. 2011

Journal of Cell Science

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“…The unique properties of Hydra ECM provide the necessary rigidity for maintenance of body shape while at the same time permitting sufficient plasticity to allow extensive but reversible shape changes along the longitudinal and radial axis. Studies by Shostak et al, (1965) showed that when isolated Hydra ECM was stretched to twice its original length, it would retract to its original length when released from tension. In this regard, it was noted in the ultrastructural studies of Davis and Haynes (1968) that in a contracted state, the fibrils of the central fibrous zone become irregular and fold upon themselves.…”

Section: Fig 1 the Hydra Body Plan Is Formed Of An Epithelial Bilaymentioning

confidence: 99%

Components, structure, biogenesis and function of the Hydra extracellular matrix in regeneration, pattern formation and cell differentiation

Sarras

2012

Int. J. Dev. Biol.

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The body wall of Hydra is organized as an epithelial bilayer (ectoderm and endoderm) with an intervening extracellular matrix (ECM), termed mesoglea by early biologists. Morphological studies have determined that Hydra ECM is composed of two basal lamina layers positioned at the base of each epithelial layer with an intervening interstitial matrix. Molecular and biochemical analyses of Hydra ECM have established that it contains components similar to those seen in more complicated vertebrate species. These components include such macromolecules as laminin, type IV collagen, and various fibrillar collagens. These components are synthesized in a complicated manner involving cross-talk between the epithelial bilayer. Any perturbation to ECM biogenesis leads to a blockage in Hydra morphogenesis. Blockage in ECM/cell interactions in the adult polyp also leads to problems in epithelial transdifferentiation processes. In terms of biophysical parameters, Hydra ECM is highly flexible; a property that facilitates continuous movements along the organism's longitudinal and radial axis. This is in contrast to the more rigid matrices often found in vertebrates. The flexible nature of Hydra ECM can in part now be explained by the unique structure of the organism's type IV collagen and fibrillar collagens. This review will focus on Hydra ECM in regard to: 1) its general structure, 2) its molecular composition, 3) the biophysical basis for the flexible nature of Hydra's ECM, 4) the relationship of the biogenesis of Hydra ECM to regeneration of body form, and 5) the functional role of Hydra ECM during pattern formation and cell differentiation.

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“…As a result, epithelial cells do not stay at the same position in the body column but change their position constantly. Shostak et al, (1965) carried out grafting between two polyps that belong to different strains, one of them being vitally labeled in both epithelium in order to visualize the movements of the grafted tissues. Interestingly they noticed that the boundaries of the labeled ectoderm and the boundaries of the labeled endoderm did not stay adjacent to each other but with time became more distant from each other, demonstrating that the speed of the movement of the epithelial cells is not the same in the two layers.…”

Section: Construction Of Ecto/endo Chimeramentioning

confidence: 99%

Transplantation analysis of developmental mechanisms in Hydra

Shimizu¹

2012

Int. J. Dev. Biol.

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To this end, they collected in several areas of Japan multiple Hydra strains that they subsequently characterized and crossed. They also established a lateral transplantation strategy that was much more powerful than the previous ones, as it combined quantitative measurements with cellular analyses thanks to the chimera procedures developed by Campbell and colleagues. Indeed this approach provided a paradigm to quantify in any morphological phenotype the Head Activation and Head Inhibition levels along the body column. In this article, I review the various strains identified by Sugiyama and colleagues, the principles and the main results deduced from the quantitative lateral transplantation strategy. In addition, I briefly discuss the relevance of this approach in the era of molecular biology.

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The role of mesoglea in mass cell movement in Hydra

Cited by 83 publications

References 14 publications

In vivo imaging of basement membrane movement: ECM patterning shapesHydrapolyps

In vivo imaging of basement membrane movement: ECM patterning shapesHydrapolyps

Components, structure, biogenesis and function of the Hydra extracellular matrix in regeneration, pattern formation and cell differentiation

Transplantation analysis of developmental mechanisms in Hydra

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