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Chondroitin Sulfate Safety and Quality

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Chondroitin Sulfate Safety and Quality molecules Review Chondroitin Sulfate Safety and Quality Nicola Volpi Department of Life Sciences, Laboratory of Biochemistry and Glycobiology, University of Modena and Reggio Emilia, 41125 Modena, Italy; [email protected]; Tel.: +39-59-2055543; Fax: +39-59-2055548 Academic Editor: Cédric Delattre Received: 7 March 2019; Accepted: 9 April 2019; Published: 12 April 2019 Abstract: The industrial production of chondroitin sulfate (CS) uses animal tissue sources as raw material derived from different terrestrial or marine species of animals. CS possesses a heterogeneous structure and physical-chemical profile in different species and tissues, responsible for the various and more specialized functions of these macromolecules. Moreover, mixes of different animal tissues and sources are possible, producing a CS final product having varied characteristics and not well identified profile, influencing oral absorption and activity. Finally, different extraction and purification processes may introduce further modifications of the CS structural characteristics and properties and may lead to extracts having a variable grade of purity, limited biological effects, presence of contaminants causing problems of safety and reproducibility along with not surely identified origin. These aspects pose a serious problem for the final consumers of the pharmaceutical or nutraceutical products mainly related to the traceability of CS and to the declaration of the real origin of the active ingredient and its content. In this review, specific, sensitive and validated analytical quality controls such as electrophoresis, eHPLC (enzymatic HPLC) and HPSEC (high-performance size-exclusion chromatography) able to assure CS quality and origin are illustrated and discussed. Keywords: chondroitin sulfate; glycosaminoglycans; osteoarthritis; nutraceuticals; food supplements 1. Chondroitin Sulfate Structure Hyaluronic acid (HA), keratan sulfate (KS), chondroitin sulfate (CS)/dermatan sulfate (DS) and heparan sulfate (HS)/heparin are natural macromolecules and the main complex heteropolysaccharides belonging to the class of glycosaminoglycans (GAGs) [1,2]. Apart from KS, which is composed of galactose and N-acetyl-d-galactosamine (GalNAc) [3], the backbone of the other GAGs is commonly represented by typical disaccharide sequences constituted of alternating units of uronic acids, glucuronic (GlcA) or iduronic (IdoA), and amino sugars, N-acetyl-d-glucosamine (GlcNAc) or GalNAc [4]. KS, CS/DS and HS/heparin are sulfated macromolecules possessing different degrees of charge density thanks to the presence of sulfate groups in varying amounts and located in different positions. Moreover, besides the variability in sulfate groups, these polysaccharides are very heterogeneous in terms of molecular mass, physicochemical properties, and biological and pharmacological properties [1–4]. CS with different disaccharides and overall carbohydrate backbones may be biosynthesized possessing various number and position of sulfate groups [4] (Figure1). Consequently, CS is a largely heterogeneous GAG formed of alternate and variously sulfated disaccharides of GlcA and GalNAc linked by β(1 3) bonds. Moreover, the different disaccharides are linked to each other by β(1 4) ! ! bonds. CSA and CSC are constituted by disaccharides sulfated in position C4 or C6 of the GalNAc residue, respectively, and minor percentages of the monosulfated disaccharide on C2 of GlcA are possible. Besides the main presence of these two kinds of disaccharide units monosulfated in position C4 or C6 of GalNAc, disaccharides with a different number and position of sulfate groups can be present, in various percentages, within the carbohydrate chains [4–6]. Various kinds of disulfated disaccharides may be present in the CS structure in various amounts also in relation to specific animal Molecules 2019, 24, 1447; doi:10.3390/molecules24081447 www.mdpi.com/journal/molecules Molecules 2019, 24, x FOR PEER REVIEW 2 of 13 C4 or C6 of GalNAc, disaccharides with a different number and position of sulfate groups can be Molecules 2019, 24, 1447 2 of 13 present, in various percentages, within the carbohydrate chains [4–6]. Various kinds of disulfated disaccharides may be present in the CS structure in various amounts also in relation to specific animal sourcessources (as (as in in cartilaginous cartilaginous or or bony bony fishes, fishes, seesee below),below), such as as the the disaccharide disaccharide disulfated disulfated in inposition position C2C2 of GlcAof GlcA and and C6 C6 of GalNAcof GalNAc (the (the so-called so-called disaccharide disaccharide D), D), in in position position C4 C4 and and C6 C6 of of the the GalNAc GalNAc unit (theunit disaccharide (the disaccharide E) or C2 E) ofor GlcAC2 of GlcA and C4 and of C4 GalNAc of GalNAc (the (the disaccharide disaccharide B) (FigureB) (Figure1). 1). Finally, Finally, a lowa low percentage of the non-sulfated disaccharide is almost always present in the CS backbone while percentage of the non-sulfated disaccharide is almost always present in the CS backbone while the the fully tri-sulfated disaccharide is generally in trace amount [4–6]. fully tri-sulfated disaccharide is generally in trace amount [4–6]. Figure 1. Structure of the disaccharides present in chondroitin sulfate backbone constituted of d-glucuronicFigure 1. Structure acid and ofN -acetyl-the disaccharidesd-galactosamine present linked in chondroitin by β(1 sulfate3) bonds. backbone The various constituted disaccharides of D- ! areglucuronic linked each acid other and by N-acetyl-β(1 4)D-galactosamine linkages. Minor linked percentages by β(1→ of3) verybonds. rare The disaccharides various disaccharides may also are have ! a sulfatelinked group each other in position by β(1→ C34) oflinkages. the glucuronic Minor percentages acid. Ac, acetylof very group. rare disaccharides may also have a sulfate group in position C3 of the glucuronic acid. Ac, acetyl group. Besides the above-illustrated CS structures, a peculiar CS polysaccharide known as CSB or DS is knownBesides in nature, the formed above-illustrated of disaccharide CS structures, units of a IdoApeculiar and CS GalNAc polysaccharide mainly sulfatedknown as in CSB position or DS C4 withis aknown minor in and nature, variable formed content of disaccharide of the disulfated units of IdoA disaccharide and GalNAc in position mainly C4sulfated of GalNAc in position and C4 C2 of IdoUAwith [a4 ].minor However, and variable the biosynthetic content of the processes disulfated generally disaccharide produce in position highly C4 modified of GalNAc oligosaccharide and C2 of IdoUA [4]. However, the biosynthetic processes generally produce highly modified oligosaccharide domains separated by regions having a low-degree of structural modifications introducing further domains separated by regions having a low-degree of structural modifications introducing further heterogeneity. Consequently, the CS and DS chains may be hybrid polymers of low modified (CS) and heterogeneity. Consequently, the CS and DS chains may be hybrid polymers of low modified (CS) highly modified (DS) domains [4]. The sulfation heterogeneity introduces a great variability in the and highly modified (DS) domains [4]. The sulfation heterogeneity introduces a great variability in positionthe position of sulfate of groups sulfate and groups in CS chargeand in density.CS charge Moreover, density. the Moreover, different numberthe different of disaccharide number unitsof formingdisaccharide the CS units polymer forming and the CS overall polymer molecular and the weight overall generatedmolecular weight are other generated key factors are other influencing key its properties.factors influencing Finally, its theproperties. combination Finally, of the the combination different sulfated of the different disaccharides sulfated anddisaccharides oligosaccharide and domainsoligosaccharide produces domains a huge produces number ofa huge heterogeneous number of heterogeneous CS polymers CS possessing polymers possessing various, specific various, and specializedspecific and biological specialized and biological pharmacological and pharmacological functions [1, 2functions]. [1,2]. 2. Chondroitin2. Chondroitin Sulfate Sulfate Activity Activity CSCS is ais naturala natural biomacromolecule biomacromolecule abundantlyabundantly distributed in in virtually virtually all all invertebrates invertebrates and and vertebratesvertebrates (and (and consequently consequently in in humans) humans) and and involved involved in in many many biological biological processes processes [ 1[1,5,7,8].,5,7,8]. BasedBased on its organism-to-organismon its organism-to-organism and tissue-to-tissue and tissue-to-tissue structural structural diversity diversity in chain in lengthchain length and sulfation and sulfation patterns, CSpatterns, provides CS specific provides biological specific functionsbiological atfunctions molecular, at molecular, cellular and cellular organ and level organ such level as such cell adhesion,as cell celladhesion, division andcell didivisionfferentiation, and differentiation, morphogenesis, morphogenesis, organogenesis organogenesis and neural network and neural formation network [9–11 ]. Moreover,formation CS [9–11]. is particularly Moreover, abundant CS is particularly in all mammalian abundant connective in all mammalian tissues, especially connective in the tissues, cartilage, skin,especially blood vessels, in the ligamentscartilage, skin, and tendonsblood vessels, with di ligamentsfferent structure and tendons and level with
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