Purification and characterisation of a minor low-sulphated
dermatan sulphate-proteoglycan from ray skin
Costas C. Chatziioannidis, Nikos K. Karamanos,
Stavros T. Anagnostides, Theodore Tsegenidis*
Section of Organic Chemistry, Biochemistry and Natural Products,
Department of Chemistry, University of Patras, 26500 Patras, Greece
(Received 21 May 1998; accepted 4 March 1999)
Abstract — A minor low-sulphated dermatan sulphate proteoglycan was isolated from ray skin by extraction with 2% sodium dodecyl
sulphate, followed with ion-exchange chromatography, gel chromatography and density gradient centrifugation. The proteoglycan
with a relative molecular mass (M
r
) ranging from 70 to 120 kDa is composed of about two dermatan sulphate chains (M
r
33 kDa)
bound on a protein core of M
r
27 kDa, and oligosaccharides consisting of uronic acids, hexosamines and neutral sugars. The major
amino acids of the protein core were glycine (corresponding to about one-fourth of the total amino acids), serine, threonine, glutamic
acid/glutamine, leucine and cysteine, together amounting to 56% of the total. The isolated proteoglycan does not interact with
hyaluronic acid and does not form self-aggregates. Dermatan sulphate was rich in iduronic acid (62% of total uronic acid) and
composed of non-sulphated (44%), and mono-sulphated disaccharides bearing esterified sulphate groups at positions C-4 (53%) or C-6
(3%) of the N-acetyl galactosamine. HPLC analysis of a pure preparation of dermatan sulphate, showed the presence of galactose and
glucose possibly as branches on the dermatan sulphate chain. © Société française de biochimie et biologie moléculaire / Elsevier, Paris
proteoglycans / dermatan sulphate / ray skin
1. Introduction
Dermatan sulphate-containing proteoglycans are
widely distributed in the extracellular matrix of skin and a
variety of other connective tissues [1–4]. The predominant
proteoglycan (PG) found in vertebrate skin is decorin,
which consists of a protein core of 329 amino acids [5]
carrying a single dermatan sulphate (DS) chain [6] and
three N-linked oligosaccharides [7]. A small dermatan
sulphate-proteoglycan (biglycan), which carries two der-
matan sulphate chains and two N-linked oligosaccharides
on a core of the same size as decorin’s, was isolated from
cultured fibroblasts [8] and from most adult fibrous con-
nective tissues [9]. Skin also contains a large chondroitin
sulphate-proteoglycan (versican) in small amounts [10,
11]. Studies on chondrichthyes, which are primitive ver-
tebrate organisms, have established that shark skin con-
tains hyaluronic acid (HA), DS, over-sulphated DS and
chondroitin sulphate (CS) [12], chimaera skin contains
HA and CS [13], while ray skin showed the presence of
DS, very low-sulphated DS (LSDS) and trace amounts of
HA [14].
A major proteoglycan, DSI-PG, was isolated from ray
skin recently, bearing one dermatan sulphate chain with
slightly increased degree of sulphation and oligosaccha-
rides containing uronic acid (Chatziioannidis et al., sub-
mitted). DSI-PG was almost completely extracted from
the tissue by 4 M guanidine hydrochloride (GdnHCl),
containing 1.5% Triton X-100 and separated from other
possible minor proteoglycans by ion-exchange chroma-
tography. DS chains contain significant amounts of disul-
phated disaccharides (Δdi-diS) with high variability in the
position of sulphation and of neutral monosaccharides.
High variability in sulphate distribution [15–17] as well as
in the presence of neutral sugar branches [15, 18–23] has
also been found in some glycosaminoglycans (GAGs)
present in invertebrates. In addition, DSI-PG showed a
variation on the protein core size. It was, further, identified
that the protein core does not have any similarity with
those of small leucine-rich repeat proteoglycans.
In the present work the extraction from ray skin (Raja
clavata), purification and characterisation of a minor small
proteoglycan bearing low-sulphated dermatan sulphate
chains is reported. It is also demonstrated that this PG
does not interact with hyaluronic acid and does not form
self-aggregates.
* Correspondence and reprints
Abbreviations: HPLC, high-performance liquid chromatogra-
phy; PGs, proteoglycans; GAGs, glycosaminoglycans; CS,
chondroitin sulphate; DS, dermatan sulphate; HA, hyaluronic
acid; LSDS, very low-sulphated dermatan sulphate; Δdi-diS,
Δ-disaccharides containing two sulphate groups; GdnHCl, gua-
nidine hydrochloride; SDS, sodium dodecyl sulphate; PMSF,
phenylmethanesulphonyl fluoride; NEM, N-ethyl maleimide.
Biochimie 81 (1999), 187-196
© Société française de biochimie et biologie moléculaire / Elsevier, Paris