<i>Hydra</i> and Niccolo Paganini (1782–1840)—two peas in a pod? The molecular basis of extracellular matrix structure in the invertebrate, <i>Hydra</i>

Sarras, Michael P.; Deutzmann, Rainer

doi:10.1002/bies.1101

Cited by 43 publications

(28 citation statements)

References 55 publications

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“…As noted by Deutzmann et al (2000), in the human-type VII-Ehlers-Danlos syndrome, the lack of processing of the N-propeptide in type I molecules alters the formation of fibrils, which become thin and irregular, resulting in joint and skin abnormalities. Hydra ECM is a highly elastic matrix, and the structural features of hydra fibrillar collagens partially mimic the physical state of the matrix of this Ehlers-Danlos syndrome (Sarras and Deutzmann, 2001). As indicated above, the low level of proline residues in the main triple helix of hydra collagen also supports the concept of a more flexible molecule.…”

Section: )mentioning

confidence: 99%

“…This group of sponges is considered to be a more evolved branch of the phylum, and, unlike the others, it possesses spermatozoa with acrosomes. In another diploblastic phylum, Cnidarian, the subepithelial zones of the mesoglae resemble vertebrate basal laminae, and a type IV collagen chain has been characterized in hydra Sarras and Deutzmann, 2001). In vertebrates, six type IV chains have been characterized and the corresponding genes are arranged pairwise (COL4A1-COL4A2, COL4A3-COL4A4, and COL4A5-COL4A6) in a head-to-head fashion on three different chromosomes (Hudson et al, 1993).…”

Section: Spongin: a Collagen Family At The Origin Of Vertebrate Nonfimentioning

confidence: 99%

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Evolution of collagens

et al. 2002

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The extracellular matrix is often defined as the substance that gives multicellular organisms (from plants to vertebrates) their structural integrity, and is intimately involved in their development. Although the general functions of extracellular matrices are comparable, their compositions are quite distinct. One of the specific components of metazoan extracellular matrices is collagen, which is present in organisms ranging from sponges to humans. By comparing data obtained in diploblastic, protostomic, and deuterostomic animals, we have attempted to trace the evolution of collagens and collagen-like proteins. Moreover, the collagen story is closely involved with the emergence and evolution of metazoa. The collagen triple helix is one of numerous modules that arose during the metazoan radiation which permit the formation of large multimodular proteins. One of the advantages of this module is its involvement in oligomerization, in which it acts as a structural organizer that is not only relatively resistant to proteases but also permits the creation of multivalent supramolecular networks. Anat Rec 268: 302-316, 2002.

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Section: )mentioning

confidence: 99%

Section: Spongin: a Collagen Family At The Origin Of Vertebrate Nonfimentioning

confidence: 99%

Evolution of collagens

et al. 2002

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“…The ECM in Hydra is a porous collagenous layer that maintains together the two epithelial cell layers, providing thus the shape but also the resistance and the flexibility of the animal (Sarras and Deutzmann, 2001;Shimizu et al, 2008). The questions raised by Michael Sarras in this issue are centered on two main issues: what are the biochemical properties that provide this unusual flexible and elastic structure, and what function(s) is playing the ECM on the amazing developmental potential of Hydra (Sarras, 2012).…”

Section: The Importance Of the Extra-cellular Matrix (Ecm) In Developmentioning

confidence: 99%

Hydra, a fruitful model system for 270 years

Galliot¹

2012

Int. J. Dev. Biol.

152

113

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The discovery of Hydra regeneration by Abraham Trembley in 1744 promoted much scientific curiosity thanks to his clever design of experimental strategies away from the natural environment. Since then, this little freshwater cnidarian polyp flourished as a potent and fruitful model system. Here, we review some general biological questions that benefitted from Hydra research, such as the nature of embryogenesis, neurogenesis, induction by organizers, sex reversal, symbiosis, aging, feeding behavior, light regulation, multipotency of somatic stem cells, temperature-induced cell death, neuronal transdifferentiation, to cite only a few. To understand how phenotypes arise, theoricists also chose Hydra to model patterning and morphogenetic events, providing helpful concepts such as reaction-diffusion, positional information, and autocatalysis combined with lateral inhibition. Indeed, throughout these past 270 years, scientists used transplantation and grafting experiments, together with tissue, cell and molecular labelings, as well as biochemical procedures, in order to establish the solid foundations of cell and developmental biology. Nowadays, thanks to transgenic, genomic and proteomic tools, Hydra remains a promising model for these fields, but also for addressing novel questions such as evolutionary mechanisms, maintenance of dynamic homeostasis, regulation of stemness, functions of autophagy, cell death, stress response, innate immunity, bioactive compounds in ecosystems, ecotoxicant sensing and science communication. KEY WORDS: historical perspective, transplantation, modeling, developmental reactivation, Hydra regeneration, multipotency, stemness, symbiosis, environmentThe heuristic value of the Hydra model systemIn the early 18th century the word biology was not yet in use but the nature of living organisms and their evolutionary relationships was the focus of interest for philosophers and naturalists, as evidenced by their pioneering efforts to develop new tools such as microscopes that would allow finer observation (Palm, 1996). The microscopic observation of organisms taken in the field undoubtedly helped develop morphological keys to sort between the animal and vegetal kingdoms and to group them into phyla (Linnaeus, 1758). Among the ambiguous species that could not be easily classified were the seawater corals that looked like flowers (Watson, 1753;McConnell, 1990) and the freshwater Hydra polyp that was considered to exhibit both animal and vegetal features. For example, Hydra easily reproduces asexually through budding, a trait frequently assigned to plants or fungi.Having observed some Hydra polyps in a pond, Abraham Trembley (1710-1784) (who had received a PhD in mathematics from the University of Geneva (Switzerland) and was now educating the children of the Count of Bentick in the Netherlands) decided Int. J. Dev. Biol. 56: 411-423 (2012) to solve that problem by testing their capacity to regenerate, assuming that if Hydra regenerates, then it should be considered a plant, but if it does...

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“…Studies of extracellular matrix in hydra have established that it has a similar molecular composition to that seen in vertebrate species [1][2][3][4] and functional studies have established that cell-ECM interactions are critical to developmental processes in hydra [2][3][4][5][6][7][8][9][10], [45]. Hydra ECM is in a constant state of turnover [6]; thus indicating that matrix-degrading enzyme systems must be in place in hydra to execute these proteolytic processes.…”

Section: Matrix Metalloproteinase (Mmp) In Hydramentioning

confidence: 99%

“…The entire body wall of hydra is organized as a simple epithelial bilayer with an intervening extracellular matrix (ECM). Previous studies have established that hydra ECM has a similar molecular composition to that of vertebrate species [1][2][3][4][5] and functional studies have established that cell-ECM interactions are critical to developmental processes in hydra [2][3][4][5][6][7][8][9][10].The organism has about 20 different cell types that are distributed along the longitudinal axis in a specific pattern [11], [12]. For example, battery cells are restricted to the tentacle ectoderm and basal disk cells are restricted to the base of the foot process.…”

Section: Introductionmentioning

confidence: 99%

Structure, expression, and developmental function of early divergent forms of metalloproteinases in Hydra

Sarras

Li²,

Leontovich

et al. 2002

Cell Res

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Metalloproteinases have a critical role in a broad spectrum of cellular processes ranging from the breakdown of extracellular matrix to the processing of signal transduction-related proteins. These hydrolytic functions underlie a variety of mechanisms related to developmental processes as well as disease states. Structural analysis of metalloproteinases from both invertebrate and vertebrate species indicates that these enzymes are highly conserved and arose early during metazoan evolution. In this regard, studies from various laboratories have reported that a number of classes of metalloproteinases are found in hydra, a member of Cnidaria, the second oldest of existing animal phyla. These studies demonstrate that the hydra genome contains at least three classes of metalloproteinases to include members of the 1) astacin class, 2) matrix metalloproteinase class, and 3) neprilysin class. Functional studies indicate that these metalloproteinases play diverse and important roles in hydra morphogenesis and cell differentiation as well as specialized functions in adult polyps. This article will review the structure, expression, and function of these metalloproteinases in hydra.

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Hydra and Niccolo Paganini (1782–1840)—two peas in a pod? The molecular basis of extracellular matrix structure in the invertebrate, Hydra

Cited by 43 publications

References 55 publications

Evolution of collagens

Evolution of collagens

Hydra, a fruitful model system for 270 years

Structure, expression, and developmental function of early divergent forms of metalloproteinases in Hydra

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