An Extracellular Matrix Protein of Jellyfish Homologous to Mammalian Fibrillins Forms Different Fibrils Depending on the Life Stage of the Animal

Abstract

A monoclonal antibody generated against the isolated extracellular matrix (ECM) of the medusa Podocoryne carnea M. Sars (Coelenterata, Cnidaria, Hydrozoa) stains a fibrillar component of the Podocoryne ECMs in immunohistochemical preparations. The antigen shows a different staining pattern according to the type of ECMs from the animals life cycle. In ontogeny the epitope first appears after gastrulation in the planula larva as single widely dispersed small fibrils, which later accumulate to form a dense meshwork in the larval ECM. The distribution of the antigen strongly suggests an important role of the molecule to cover the biomechanical needs of the animal. In immunoblots one band with a size of 330 kDa is detectable in the polyp ECM, whereas in the outer ECM of the medusa a 340-kDa band is observed. Both the 330- and the 340-kDa bands appear when probed on the inner ECM of the medusa or on ECMs of the larva. The antibody was used to isolate a cDNA clone from an expression library. The deduced amino acid sequence of this cDNA fragment reveals a molecular structure composed of tandemly repeated epidermal growth factor-like repeats interrupted by a second cystein-rich motif first found in the latent transforming growth factor beta binding protein. Comparison of the sequence to the data bases indicates < 40% identity to human fibrillins. The presence of fibrillin-like beaded microfibrils in the ECM of P. carnea is furthermore demonstrated by electron microscopy after rotary shadowing. Our results demonstrate for the first time the existence of this noncollagenous interstitial ECM protein in invertebrates and suggest that the structure and the function of fibrillin have been conserved during evolution.

The modulus of elasticity of fibrillin-containing elastic fibres in the mesoglea of the hydromedusaPolyorchis penicillatus

“…Fibres were oriented more or less perpendicularly to the exand sub-umbrellar surfaces and traversed most of the thickness of the bell, anchored in the exumbrella by intertwining with the fibres there, as observed by other workers (Gladfelter, 1972;Weber and Schmid, 1985;Reber-Müller et al, 1995). Near the gastrodermal lamella, they branched multiply into finer and finer fibres, presumably anchoring themselves in the lamella, though this could not be discerned using the available microscope.…”

“…The fibres are multiply branched at each end and intertwine with the tissue layers to provide solid connections. Weber and Schmid (1985) showed these fibres to be microfibril bundles, and Reber-Müller et al (1995) showed them to be rich in fibrillin. These fibres are reported to be 1.5-1.8·m in diameter in fixed Polyorchis tissue samples (Gladfelter, 1972;Weber and Schmid, 1985), 0.03-1·m in Limnocnida and 2-3·m in Pelagia and Aurelia (Bouillon and Vandermeerssche, 1957).…”

“…Hydrozoan mesoglea is a hydrogel that contains mucopolysaccharides, collagen fibrils and other structural proteins, including microfibrils rich in a protein homologous to mammalian fibrillin (Bouillon and Vandermeerssche, 1957;Bouillon and Coppois, 1977;Gladfelter, 1972;Weber and Schmid, 1985;Reber-Müller et al, 1995). Fibrillar collagen type IV, fibronectin and heparansulfate proteoglycan have been reported from the mesoglea of Hydra sp.…”

“…In the outer layer -the so-called 'bell mesoglea' -there is a radially arranged array of larger diameter fibres, which extend from the gastrodermal lamella to the exumbrellar epithelium (Chapman, 1959;Gladfelter, 1972;Weber and Schmid, 1985;DeMont, 1986;Reber-Müller et al, 1995. The fibres are multiply branched at each end and intertwine with the tissue layers to provide solid connections.…”

“…Bouillon and Coppois (1977) showed that they could be made to stain for elastin, which led them to conclude that they are analogous in structure to vertebrate elaunin fibres, described by Kielty et al (2002) as consisting of an outer microfibrillar sheath and an inner core of amorphous crosslinked elastin. However, since elastin seems to be limited to the vertebrates (Faury, 2001), Reber-Müller et al (1995 speculated that there might well be an as yet unidentified elastic protein in the radial fibres. Similar speculation led Shadwick and Gosline (1985) to their discovery of octopus arterial elastomer (OAE), an analogous elastin-like protein in the circumferential fibres of octopus aorta.…”