The Collagen of the Porifera

Garrone, R.

doi:10.1007/978-1-4684-7636-1_12

Cited by 30 publications

(26 citation statements)

References 13 publications

(12 reference statements)

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“…The information available for collagen fibrils is in full agreement with results from several studies [16,21,231. It shows, in addition, fine filaments associated with the surface of the fibrils, a feature rarely pointed out [29, 311.…”

Section: Discussionsupporting

confidence: 88%

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A six‐armed, tenascin‐like protein extracted from the Porifera Oscarella tuberculata (Homosclerophorida)

Humbert-David

Garrone

1993

European Journal of Biochemistry

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A six-armed complex could be extracted from the marine sponge Osccrrellu tuberculuta by a two-step incubation, first in Tris-buffered saline containing EDTA, then in Tris-buffered saline containing urea. The crude extracts contained, in addition, collagen fibrils with surface filaments, individual filaments resembling collagen molecules, and laminidnidogen-like complexes. The extracts were subsequently purified by gel-filtration chromatography and low-pressure ion-exchange chromatography on DEAE-cellulose, then analyzed by SDS/PAGE and iinmunoblotting methods. A glycoprotein of high molecular mass was isolated, and reduced to subunits of 230 kDa. After transfer to nitrocellulose, both the complex and its subunits were faintly stained by antibodies against amphibian tenascin. Electron microscopy of the purified extracts demonstrated the presence of a large population of tenascin-like molecules and complexes of several molecules interacting with each other by their central globule.Tenascin (also known as hexabrachion, cytotactin, J1, myotendinous antigen) is a large extracellular-matrix glycoprotein containing six similar disulfide-linked subunits which give the protein a characteristic six-armed structure when visualized by electron microscopy ([l-31 for review). It has a distinctive tissue distribution during development [4, 51 and several reports described both its adhesive and anti-adhesive properties (reviewed in [6, 71). Recent studies indicate that the promoter of the tenascin gene contains target regions responding to homeodomain proteins, suggesting that tenascin could be a morphoregulatory molecule 18, 91. However, the crucial role of tenascin during development has been questioned by recent data. Homologous recombination experiments produced mutant mice in which tenascin gene expression was disrupted, but the homozygous null-mutant mice had apparently no defect [lo], at least under resting conditions.Tenascin has been characterized in several vertebrate groups, including Amphibians [ll]. Its presence has been also demonstrated in leech, where it promotes neurite outgrowth [12, 131. Tenascin-like proteins have been localized in sea-urchin embryos [14], and two genes related to tenascin have been detected in Drusophilu: Ten' [15] and Ten"' (Baumgartner, S . , unpublished results).In the course of our research program on the evolution of the extracellular matrix, we have investigated the presence of basement-membrane molecules in Porifera. The Porifera constitute the most primitive phylum of multicellular animals. They possess an extended extracellular matrix [16] containing at least two types of collagen [17-191, However, a group of marine sponges, the Homosclerophorida, possess laminae underlying their epithelia which resemble basement membranes [23]. These sponges have a simplified organization which is sometimes considered as a result of an evolutionary process [24]. Pieces of Oscurellu where treated in order to extract laminin, an adhesive glycoprotein of basement membranes, according to an efficie...

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Section: Discussionsupporting

confidence: 88%

“…The Porifera constitute the most primitive phylum of multicellular animals. They possess an extended extracellular matrix [16] containing at least two types of collagen [17-191, [21]. They lack highly differentiated tissues [22] and basement membranes [16], at least in most species.…”

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confidence: 99%

A six‐armed, tenascin‐like protein extracted from the Porifera Oscarella tuberculata (Homosclerophorida)

Humbert-David

Garrone

1993

European Journal of Biochemistry

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“…What is the function of 3Hyp residues in collagen? It is clearly an ancient post-translational modification, found in the most primitive invertebrates including sponge (Porifera) fibrillar collagens (22) and prominent in basement membrane type IV collagens in which about 1 in 10 hydroxyprolines are 3Hyp (23). This implies biological benefits through a fundamental contribution to the properties of collagen structure itself.…”

Section: Discussionmentioning

confidence: 99%

A Novel 3-Hydroxyproline (3Hyp)-rich Motif Marks the Triple-helical C Terminus of Tendon Type I Collagen

Eyre

Weis

Hudson

et al. 2011

Journal of Biological Chemistry

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Because of its unique physical and chemical properties, rat tail tendon collagen has long been favored for crystallographic and biochemical studies of fibril structure. In studies of the distribution of 3-hydroxyproline in type I collagen of rat bone, skin, and tail tendon by mass spectrometry, the repeating sequences of Gly-Pro-Pro (GPP) triplets at the C terminus of ␣1(I) and ␣2(I) chains were shown to be heavily 3-hydroxylated in tendon but not in skin and bone. By isolating the tryptic peptides and subjecting them to Edman sequence analysis, the presence of repeating 3-hydroxyprolines in consecutive GPP triplets adjacent to 4-hydroxyproline was confirmed as a unique feature of the tendon collagen. A 1960s study by Piez et al. (Piez, K. A., Eigner, E. A., and Lewis, M. S. (1963) Biochemistry 2, 58 -66) in which they compared the amino acid compositions of rat skin and tail tendon type I collagen chains indeed showed 3-4 residues of 3Hyp in tendon ␣1(I) and ␣2(I) chains but only one 3Hyp residue in skin ␣1(I) and none in ␣2(I). The present work therefore confirms this difference and localizes the additional 3Hyp to the GPP repeat at the C terminus of the triple-helix. We speculate on the significance in terms of a potential function in contributing to the unique assembly mechanism and molecular packing in tendon collagen fibrils and on mechanisms that could regulate 3-hydroxylation at this novel substrate site in a tissuespecific manner.Prolyl 3-hydroxylation, a long recognized quantitatively minor post-translational modification of collagen (1), has received much attention in the last few years after gene mutations affecting its formation were found to cause recessive forms of osteogenesis imperfecta (2-5). A single primary site of 3-hydroxyproline (3Hyp) 2 is present in normal collagen ␣1(I) and ␣1(II) chains at Pro-986 of the triple-helix (6, 7) but is not hydroxylated in the tissues of mice and humans with recessive osteogenesis imperfecta caused by mutations in CRTAP or LEPRE1 (the gene encoding P3H1) (2-5). The LEPRE1 gene encodes P3H1, which is one of three prolyl 3-hydroxylases (P3H1, P3H2, and P3H3) in the mammalian genome. CRTAP encodes a protein that is homologous to the N-terminal half of P3H1, which it associates with P3H1 together with cyclophilin B to form the functional enzyme complex required for Pro-986 3-hydroxylation of unfolded collagen chains in the endoplasmic reticulum (8).We recently identified several other sites of prolyl 3-hydroxylation in fibrillar collagen chains including Pro-707 in ␣2(I) and ␣2(V), Pro-944 in ␣1(II) and ␣2(V), Pro-470 in ␣2(V), and Pro-434, Pro-665, and Pro-692 in ␣1(V), ␣1(XI), and ␣2(XI) but a lack of any 3-hydroxyproline in the mammalian ␣1(III) chain (7). The D-periodic spacing between three of these additional sites in clade A collagen chains (␣1(I), ␣2(I), ␣1(II), and ␣2(V)) and between two in clade B (␣1(V), ␣1(XI), and ␣2(XI)) suggested a role in fibril formation. In pursuing this concept further, we investigated the potential for differences in 3-hydrox...

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“…Genomic and complementary DNA studies showed that both proteinaceous fibrous materials contain the classic collagenous Gly-Xaa-Yaa motif (Exposito and Garrone, 1990;Boute et al, 1996). The existence of collagen in marine as well as in freshwater sponges was first proved electron microscopically (Garrone, 1985;Diehl-Seifert et al, 1995); later the corresponding genes were cloned. A cDNA encoding a short-chain collagen (Exposito and Garrone, 1990) and a cDNA for collagen type IV, which is characteristic for basal laminae (Boute et al, 1996), have been identified.…”

Section: Introductionmentioning

confidence: 99%

Prolidase in the Marine Sponge Suberites domuncula: Enzyme Activity, Molecular Cloning, and Phylogenetic Relationship

et al. 1999

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: The enzyme prolidase hydrolyzes the peptide bond that involves the imino nitrogen of proline or hydroxyproline; hence, it catalyzes the final step in collagen degradation. From mammals it is known that this enzyme plays a major role in the recycling of proline for collagen synthesis and can be considered to be essential for the control of cell growth. The dominant organic exoskeleton in sponges, especially in Demospongiae, is collagen and the collagen-related spongin. Here we demonstrate that crude extracts of the demosponge Suberites domuncula contain prolidase or prolidase-like activity. The complementary DNA encoding the putative prolidase was cloned from a library of the same animal. Two different forms of cDNAs, termed SDPEPD1 and SDPEPD2, were identified, coding for the putative polypeptides PEPD_SD-1 with a molecular mass of 55,805 Da and PEPD_SD-2 with 51,684. Evidence is presented suggesting that the two different transcripts originate from the same gene but are formed by an alternative splicing event. We conclude that demosponges contain the activity as well as the gene for prolidase, a major enzyme involved in collagen metabolism, spicule formation, and cell motility. Phylogenetic analysis revealed that the sponge prolidase branches off first from the common ancestor of metazoan prolidases and later than the yeast prolidase; only distantly related are the bacterial enzymes.

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The Collagen of the Porifera

Cited by 30 publications

References 13 publications

A six‐armed, tenascin‐like protein extracted from the Porifera Oscarella tuberculata (Homosclerophorida)

A six‐armed, tenascin‐like protein extracted from the Porifera Oscarella tuberculata (Homosclerophorida)

A Novel 3-Hydroxyproline (3Hyp)-rich Motif Marks the Triple-helical C Terminus of Tendon Type I Collagen

Prolidase in the Marine Sponge Suberites domuncula: Enzyme Activity, Molecular Cloning, and Phylogenetic Relationship

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