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Medical Applications and Drawbacks molecules Review Galactosaminoglycans: Medical Applications and Drawbacks Vitor H. Pomin 1,2,* , William P. Vignovich 1, Alysia V. Gonzales 1, Ariana A. Vasconcelos 3 and Barbara Mulloy 4 1 Department of Biomolecular Sciences, School of Pharmacy, University of Mississippi, Oxford, MS 38677-1848, USA 2 Research Institute of Pharmaceutical Sciences, School of Pharmacy, University of Mississippi, Oxford, MS 38677-1848, USA 3 Institute of Medical Biochemistry Leopoldo de Meis, Federal University of Rio de Janeiro, Rio de Janeiro, RJ 21941-590, Brazil 4 Imperial College, Department of Medicine, Burlington Danes Building, Du Cane Road, London W12 0NN, UK * Correspondence: [email protected] Academic Editors: Giangiacomo Torri, Jawed Fareed and Job Harenberg Received: 19 June 2019; Accepted: 30 July 2019; Published: 1 August 2019 Abstract: Galactosaminoglycans (GalAGs) are sulfated glycans composed of alternating N-acetylgalactosamine and uronic acid units. Uronic acid epimerization, sulfation patterns and fucosylation are modifications observed on these molecules. GalAGs have been extensively studied and exploited because of their multiple biomedical functions. Chondroitin sulfates (CSs), the main representative family of GalAGs, have been used in alternative therapy of joint pain/inflammation and osteoarthritis. The relatively novel fucosylated chondroitin sulfate (FCS), commonly found in sea cucumbers, has been screened in multiple systems in addition to its widely studied anticoagulant action. Biomedical properties of GalAGs are directly dependent on the sugar composition, presence or lack of fucose branches, as well as sulfation patterns. Although research interest in GalAGs has increased considerably over the three last decades, perhaps motivated by the parallel progress of glycomics, serious questions concerning the effectiveness and potential side effects of GalAGs have recently been raised. Doubts have centered particularly on the beneficial functions of CS-based therapeutic supplements and the potential harmful effects of FCS as similarly observed for oversulfated chondroitin sulfate, as a contaminant of heparin. Unexpected components were also detected in CS-based pharmaceutical preparations. This review therefore aims to offer a discussion on (1) the current and potential therapeutic applications of GalAGs, including those of unique features extracted from marine sources, and (2) the potential drawbacks of this class of molecules when applied to medicine. Keywords: Carbohydrate-based drug discovery; chondroitin sulfate; dermatan sulfate; fucosylated chondroitin sulfate; galactosaminoglycans 1. Introduction Galactosaminoglycan (GalAG) is a term specifically used to designate the classes and sub-classes of glycosaminoglycans (GAGs) that contain N-acetylgalactosamine (GalNAc) units as the hexosamine type in their repeating disaccharide building blocks. In addition to the GalNAc unit, the disaccharide blocks of these high molecular weight (MW) polymers are additionally composed of an uronic acid, which can be either β-d-glucuronic acid (GlcA) or its C5 epimer, α-l-iduronic acid (IdoA) [1]. Although the GalAGs are homogeneously composed of alternating 3-linked GalNAc and 4-linked IdoA/GlcA Molecules 2019, 24, 2803; doi:10.3390/molecules24152803 www.mdpi.com/journal/molecules Molecules 2019, 24, x 2 of 34 Molecules 2019, 24, 2803 2 of 33 4-linked IdoA/GlcA units, the backbones of these glycans are extensively modified by different levels of C5 epimerization [2], sulfation contents and patterns [3,4], and in certain cases, fucosylation [5,6]units, (Figure the backbones 1). As detailed of these below, glycans the are extensivelyfucose decoration modified on by the di ffGalAGerent levels backbone of C5 epimerizationcan be further [2 ], sulfatedsulfation at contentsdifferent and positions patterns and [3, 4degrees], and in [6]. certain The cases,principal fucosylation representati [5,6ves] (Figure of GalAGs1). As detailedare the chondroitinbelow, the fucosesulfates decoration (CSs), dermatan on the GalAG sulfate backbone (DS) and can fucosylated be further chondroitin sulfated at disulfatefferent (FucCS) positions (Figureand degrees 1). Like [6 all]. The GAGs, principal GalAGs representatives are key structural of GalAGs players are of the living chondroitin organisms sulfates and are (CSs), found dermatan more commonlysulfate (DS) in andthe extracellular fucosylated chondroitinmatrix (ECM) sulfate environm (FucCS)ent or (Figure attached1). Like to the all cell GAGs, surface GalAGs than areinside key thestructural cells. players of living organisms and are found more commonly in the extracellular matrix (ECM) environment or attached to the cell surface than inside the cells. CH2OR6 CH OR ABGlcA/IdoA GlcA 2 O O R R O O - 5 4 COO RO O β(1→4) O O β(1→4) O O R5' β(1→4) β(1→4) OR 3 β/α(1→3) O β(1→3) O O NH NH O COCH 3 COCH3 OR2 CH α(1→3) OH GalNAc 3 - RO GalNAc R2, R3, R4 and R6 = H or SO3 - CS: R5 = COO and R5’ = H (β-D-GlcA) RO - - CS-A: R4 = SO3 (predominantly) and R6 = SO3 (occasionally) - - - Fucp R = H or SO3 CS-C: R4 = SO3 (occasionally) and R6 = SO3 (predominantly) OR - CS-D: R2 and R6 = SO3 (mostly) - CS-E: R4 and R6 = SO3 (predominantly) - CS-K : R3 and R4 = SO3 (predominantly) - CS-L: R3 and R6 = SO3 (predominantly) - CS-M: R3, R4 and R6 = SO3 (predominantly) - OSCS: R2, R3, R4 and R6 = SO3 (predominantly) - - CS-B or DS: R5 = H and R5’ = COO (α-L-IdoA) >> R5 = COO and R5’ = H (β-D-GlcA) - R2 and R4 = H or SO3 ; R3 and R6 = H FigureFigure 1. 1.(A(A) Representative) Representative repeating repeating disaccharide disaccharide unit ofof chondroitinchondroitin sulfate sulfate (CS) (CS) structures. structures. CSs CSs are β d β d arecomposed composed of alternating of alternating 4-linked - -glucuronic4-linked β acid-D-glucuronic (GlcA) and 3-linkedacid (GlcA)- -N-acetylgalactosamine and 3-linked β-(GalNAc)D-N-acetylgalactosamine units. While CS-A(GalNAc) is mostly units. 4-sulfatedWhile CS-A at theis mostly GalNAc 4-sulfated units, CS-Cat the is GalNAc predominantly units, CS-C6-sulfated is predominantly [7]. While CS-D 6-sulfated is composed [7]. While of 2-sulfated CS-D is GlcA composed and 6-sulfated of 2-sulfated GalNAc, GlcA CS-E and is composed6-sulfated of GalNAc,4,6-di-sulfated CS-E is GalNAc. composed CS-K, of 4,6-di-sulfated CS-L and CS-M GalNA are allc. sulfated CS-K, CS-L at C3 and position CS-M of are GlcA, all andsulfated respectively at C3 positionsulfated of at GlcA, positions and respectively C4, C6, and sulfated simultaneously at positions at C4 C4, and C6, C6. and Oversulfated simultaneously chondroitin at C4 and sulfate C6. Oversulfated(OSCS) is fully chondroitin sulfated. Dermatansulfate (OSCS) sulfate is (DS)fully alsosulfated. known Dermatan as CS-B is sulfate composed (DS) ofalso alternating known as 4-linked CS-B α-L-iduronic acid (IdoA) and 3-linked β-d-GalNAc units. (B) Representative repeating trisaccharide is composed of alternating 4-linked α-L-iduronic acid (IdoA) and 3-linked β-D-GalNAc units. (B) unit of the fucosylated chondroitin sulfate (FucCS). Besides consisting of the regular CS disaccharide Representative repeating trisaccharide unit of the fucosylated chondroitin sulfate (FucCS). Besides unit as shown at panel A, the FucCS also exhibits branching units of α-l-fucopyranose (Fucp) 3-linked consisting of the regular CS disaccharide unit as shown at panel A, the FucCS also exhibits to the GlcA unit as highlighted with the box in dashed lines. The detailed structure of the Fucp unit branching units of α-L-fucopyranose (Fucp) 3-linked to the GlcA unit as highlighted with the box in varies according to the holothurian species. In all panels the glycosidic bonds are indicated in ellipses dashed lines. The detailed structure of the Fucp unit varies according to the holothurian species. In whereas monosaccharide types are indicated in continuous black rectangles. For fast notation of the all panels the glycosidic bonds are indicated in ellipses whereas monosaccharide types are indicated sulfation patterns, sulfation sites are highlighted by light-grey rectangles. in continuous black rectangles. For fast notation of the sulfation patterns, sulfation sites are highlightedThe structural by light-grey diversity rectangles. of GalAGs directly reflects their great number of biological roles and medical uses. Examples of this wide spectrum of biological roles are cell growth and differentiation [8,9], The structural diversity of GalAGs directly reflects their great number of biological roles and morphogenesis [10,11], cell migration [12,13] and microbial infection [14]. Examples of medical medical uses. Examples of this wide spectrum of biological roles are cell growth and differentiation effects in which these molecules participate are anticoagulation [15–19], antithrombosis [20,21], [8,9], morphogenesis [10,11], cell migration [12,13] and microbial infection [14]. Examples of medical anti-inflammation [22–24], anticancer [24–26], antiviral [27–30], anti-angiogenesis [31,32] and effects in which these molecules participate are anticoagulation [15–19], antithrombosis [20,21], antimalaria [33], in addition to some beneficial effects in events of hemodialysis [34], cellular growth anti-inflammation [22–24], anticancer [24–26], antiviral [27–30], anti-angiogenesis [31,32] and modulation [35], fibrosis [36], hyperglycemia [37] and diabetes-related nephropathy [38]. Due to the antimalaria [33], in addition to some beneficial effects in events of hemodialysis [34], cellular growth many biological and medical functions of GalAGs, several scientific groups in the world are now modulation [35], fibrosis [36], hyperglycemia [37] and diabetes-related nephropathy [38]. Due to the conducting research on these molecules. Consequently, the number of publications regarding GalAGs many biological and medical functions of GalAGs, several scientific groups in the world are now has increased considerably in the last three decades. This growing interest in research about GalAGs conducting research on these molecules. Consequently, the number of publications regarding has been accompanied by the boom of glycomics [39]. The main research goals of the GalAG-related GalAGs has increased considerably in the last three decades.
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