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Glycans in Diseases and Therapeutics pp 159–184Cite as

Structure and Biological Activities of Glycosaminoglycan Analogs from Marine Invertebrates: New Therapeutic Agents?

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Part of the book series: Biology of Extracellular Matrix ((BEM))

Abstract

Although the oceans are habited by about 230,000 different animal species, only 1% of these organisms have been studied so far. Thus, the sea constitutes an immense reservoir of unique natural molecules with potential biological interest. Among the countless described compounds of marine origin, the sulfated glycosaminoglycans are a particularly interesting group of molecules. These polymers are widely distributed among different marine phyla, occurring in elevated quantities. Normally, the glycosaminoglycans from marine sources contain a high negative charge density due to the presence of sulfate groups in different positions. In addition, unique structural motifs, such as glucose and sulfated fucose branches, rarely described in glycosaminoglycans from terrestrial organisms, are also found. Various pharmacological properties ranging from anticoagulant and antithrombotic to antimetastatic and anti-inflammatory have been attributed to these molecules. The interaction and modulation of plasma coagulation proteases and inhibitors, adhesion molecules, and growth factors, among others, are the basis for their pharmacological effects. In this chapter, we review the phylogenetic distribution, the structure, and the biological effects of the marine glycosaminoglycans, as well as the molecular mechanisms involved in some of their biological activities. We also briefly discuss the possibility of using these glycans as therapeutic agents.

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Abbreviations

GalNAc:

N-acetyl galactosamine

GalNAc4S:

4-O-sulfated N-acetyl galactosamine

GalNAc4S, 6S:

4-O- and 6-O-sulfated N-acetyl galactosamine

GalNAc6S:

6-O-sulfated N-acetyl galactosamine

GlcA:

Glucuronic acid

GlcA2S:

2-O-sulfated glucuronic acid

GlcA3S:

3-O-sulfated glucuronic acid

GlcNAc:

N-acetyl glucosamine

GlcNS:

N-sulfated glucosamine

GlcNS, 3S, 6S:

N-, 3-O-, and 6-O-sulfated glucosamine

GlcNS, 6S:

N- and 6-sulfated glucosamine

HexA:

Hexuronic acid

IdoA:

Iduronic acid

IdoA2S:

2-O-sulfated iduronic acid

References

  • Alban S (2005) From heparins to factor xa inhibitors and beyond. Eur J Clin Invest 35(Suppl 1):12–20

    PubMed  CAS  Google Scholar 

  • Aletras AJ, Karamanos NK, Hjerpe A (1991) Presence of the hnk-1 epitope (3-sulfoglucuronic acid) on oligosaccharides from squid skin chondroitin proteoglycans and degradation of proteoglycans by proteolytic enzymes. Biochem Int 25(2):331–338

    PubMed  CAS  Google Scholar 

  • Ariga T, Kohriyama T, Freddo L, Latov N, Saito M, Kon K, Ando S, Suzuki M, Hemling ME, Rinehart KL Jr et al (1987) Characterization of sulfated glucuronic acid containing glycolipids reacting with igm m-proteins in patients with neuropathy. J Biol Chem 262(2):848–853

    PubMed  CAS  Google Scholar 

  • Arumugam M, Balasubramanian T, Shanmugam A, Garg H (2008) A composition study of anticoagulant and antiproliferative activity of fast moving heparin from giant clam tridacna maxima (roeding, 1798) and green mussel perna viridis (Linnaeus, 1758). J Appl Biol Sci 2(3):27–30

    CAS  Google Scholar 

  • Bao X, Pavao MS, Dos Santos JC, Sugahara K (2005) A functional dermatan sulfate epitope containing iduronate(2-o-sulfate)alpha1-3galnac(6-o-sulfate) disaccharide in the mouse brain: demonstration using a novel monoclonal antibody raised against dermatan sulfate of ascidian Ascidia nigra. J Biol Chem 280(24):23184–23193

    PubMed  CAS  Google Scholar 

  • Belmiro CL, Castelo-Branco MT, Melim LM, Schanaider A, Elia C, Madi K, Pavao MS, de Souza HS (2009) Unfractionated heparin and new heparin analogues from ascidians (chordate-tunicate) ameliorate colitis in rats. J Biol Chem 284(17):11267–11278

    PubMed  CAS  Google Scholar 

  • Bergefall K, Trybala E, Johansson M, Uyama T, Naito S, Yamada S, Kitagawa H, Sugahara K, Bergstrom T (2005) Chondroitin sulfate characterized by the e-disaccharide unit is a potent inhibitor of herpes simplex virus infectivity and provides the virus binding sites on gro2c cells. J Biol Chem 280(37):32193–32199

    PubMed  CAS  Google Scholar 

  • Borsig L, Wang L, Cavalcante MC, Cardilo-Reis L, Ferreira PL, Mourao PA, Esko JD, Pavao MS (2007) Selectin blocking activity of a fucosylated chondroitin sulfate glycosaminoglycan from sea cucumber. Effect on tumor metastasis and neutrophil recruitment. J Biol Chem 282(20):14984–14991

    PubMed  CAS  Google Scholar 

  • Bourne NF (2000) The potential for scallop culture – the next millenium. Aquac Int 8(2–3):113–122

    Google Scholar 

  • Brito AS, Arimateia DS, Souza LR, Lima MA, Santos VO, Medeiros VP, Ferreira PA, Silva RA, Ferreira CV, Justo GZ, Leite EL, Andrade GP, Oliveira FW, Nader HB, Chavante SF (2008) Anti-inflammatory properties of a heparin-like glycosaminoglycan with reduced anti-coagulant activity isolated from a marine shrimp. Bioorg Med Chem 16(21):9588–9595

    PubMed  CAS  Google Scholar 

  • Burson SL, Fahrenbach MJ, Frommhagen LH, Riccardi BA, Brown RA, Brockman JA, Lewry HV, Stokstad ELR (1956) Isolation and purification of mactins, heparin-like anticoagulants from mollusca. J Am Chem Soc 78(22):5874–5878

    CAS  Google Scholar 

  • Buyue Y, Sheehan JP (2009) Fucosylated chondroitin sulfate inhibits plasma thrombin generation via targeting of the factor ixa heparin-binding exosite. Blood 114(14):3092–3100

    PubMed  CAS  Google Scholar 

  • Cardilo-Reis L, Cavalcante MC, Silveira CB, Pavao MS (2006) In vivo antithrombotic properties of a heparin from the oocyte test cells of the sea squirt styela plicata(chordata-tunicata). Braz J Med Biol Res 39(11):1409–1415

    PubMed  CAS  Google Scholar 

  • Cassaro CM, Dietrich CP (1977) Distribution of sulfated mucopolysaccharides in invertebrates. J Biol Chem 252(7):2254–2261

    PubMed  CAS  Google Scholar 

  • Cavalcante MC, Allodi S, Valente AP, Straus AH, Takahashi HK, Mourao PA, Pavao MS (2000) Occurrence of heparin in the invertebrate styela plicata (tunicata) is restricted to cell layers facing the outside environment. An ancient role in defense? J Biol Chem 275(46):36186–36189

    Google Scholar 

  • Cavalcante MC, de Andrade LR, Du Bocage Santos-Pinto C, Straus AH, Takahashi HK, Allodi S, Pavao MS (2002) Colocalization of heparin and histamine in the intracellular granules of test cells from the invertebrate styela plicata (chordata-tunicata). J Struct Biol 137(3):313–321

    PubMed  CAS  Google Scholar 

  • Cesaretti M, Luppi E, Maccari F, Volpi N (2004) Isolation and characterization of a heparin with high anticoagulant activity from the clam tapes phylippinarum: evidence for the presence of a high content of antithrombin iii binding site. Glycobiology 14(12):1275–1284

    PubMed  CAS  Google Scholar 

  • Chavante SF, Santos EA, Oliveira FW, Guerrini M, Torri G, Casu B, Dietrich CP, Nader HB (2000) A novel heparan sulphate with high degree of n-sulphation and high heparin cofactor-II activity from the brine shrimp artemia franciscana. Int J Biol Macromol 27(1):49–57

    PubMed  CAS  Google Scholar 

  • Chou DK, Ilyas AA, Evans JE, Costello C, Quarles RH, Jungalwala FB (1986) Structure of sulfated glucuronyl glycolipids in the nervous system reacting with hnk-1 antibody and some igm paraproteins in neuropathy. J Biol Chem 261(25):11717–11725

    PubMed  CAS  Google Scholar 

  • Clement AM, Sugahara K, Faissner A (1999) Chondroitin sulfate e promotes neurite outgrowth of rat embryonic day 18 hippocampal neurons. Neurosci Lett 269(3):125–128

    PubMed  CAS  Google Scholar 

  • Conand C (2004) Present status of world sea cucumber resoruces and utilisation: an international overview. Advances in sea cucumber aquaculture and management. FAO, Rome

    Google Scholar 

  • de Barros CM, Andrade LR, Allodi S, Viskov C, Mourier PA, Cavalcante MC, Straus AH, Takahashi HK, Pomin VH, Carvalho VF, Martins MA, Pavao MS (2007) The hemolymph of the ascidian styela plicata (chordata-tunicata) contains heparin inside basophil-like cells and a unique sulfated galactoglucan in the plasma. J Biol Chem 282(3):1615–1626

    PubMed  Google Scholar 

  • Deepa SS, Umehara Y, Higashiyama S, Itoh N, Sugahara K (2002) Specific molecular interactions of oversulfated chondroitin sulfate e with various heparin-binding growth factors. Implications as a physiological binding partner in the brain and other tissues. J Biol Chem 277(46):43707–43716

    PubMed  CAS  Google Scholar 

  • Demir M, Iqbal O, Dietrich CP, Hoppensteadt DA, Ahmad S, Daud AN, Fareed J (2001) Anticoagulant and antiprotease effects of a novel heparinlike compound from shrimp (penaeus brasiliensis) and its neutralization by heparinase i. Clin Appl Thromb Hemost 7(1):44–52

    PubMed  CAS  Google Scholar 

  • Dietrich CP, de Paiva JF, Moraes CT, Takahashi HK, Porcionatto MA, Nader HB (1985) Isolation and characterization of a heparin with high anticoagulant activity from Anomalocardia brasiliana. Biochim Biophys Acta 843(1–2):1–7

    PubMed  CAS  Google Scholar 

  • Dietrich CP, Nader HB, de Paiva JF, Santos EA, Holme KR, Perlin AS (1989) Heparin in molluscs: chemical, enzymatic degradation and 13C and 1H N.M.R. Spectroscopical evidence for the maintenance of the structure through evolution. Int J Biol Macromol 11(6):361–366

    PubMed  CAS  Google Scholar 

  • Dietrich CP, Paiva JF, Castro RA, Chavante SF, Jeske W, Fareed J, Gorin PA, Mendes A, Nader HB (1999) Structural features and anticoagulant activities of a novel natural low molecular weight heparin from the shrimp Penaeus brasiliensis. Biochim Biophys Acta 1428(2–3):273–283

    PubMed  CAS  Google Scholar 

  • Dreyfuss JL, Regatieri CV, Lima MA, Paredes-Gamero EJ, Brito AS, Chavante SF, Belfort R, Farah ME, Nader HB (2010) A heparin mimetic isolated from a marine shrimp suppresses neovascularization. J Thromb Haemost 8:1828–1837

    PubMed  CAS  Google Scholar 

  • Feta A, Do AT, Rentzsch F, Technau U, Kusche-Gullberg M (2009) Molecular analysis of heparan sulfate biosynthetic enzyme machinery and characterization of heparan sulfate structure in Nematostella vectensis. Biochem J 419(3):585–593. doi:10.1042/BJ20082081

    PubMed  CAS  Google Scholar 

  • Fongmoon D, Shetty AK, Basappa YS, Sugiura M, Kongtawelert P, Sugahara K (2007) Chondroitinase-mediated degradation of rare 3-o-sulfated glucuronic acid in functional oversulfated chondroitin sulfate k and e. J Biol Chem 282(51):36895–36904

    PubMed  CAS  Google Scholar 

  • Fonseca RJ, Mourao PA (2006) Fucosylated chondroitin sulfate as a new oral antithrombotic agent. Thromb Haemost 96(6):822–829. doi:06120822 [pii]

    PubMed  CAS  Google Scholar 

  • Gandra M, Cavalcante M, Pavao M (2000) Anticoagulant sulfated glycosaminoglycans in the tissues of the primitive chordate styela plicata (tunicata). Glycobiology 10(12):1333–1340

    PubMed  CAS  Google Scholar 

  • Gandra M, Kozlowski EO, Andrade LR, de Barros CM, Pascarelli BM, Takiya CM, Pavao MS (2006) Collagen colocalizes with a protein containing a decorin-specific peptide in the tissues of the ascidian styela plicata. Comp Biochem Physiol B Biochem Mol Biol 144(2):215–222

    PubMed  Google Scholar 

  • Glauser BF, Pereira MS, Monteiro RQ, Mourao PA (2008) Serpin-independent anticoagulant activity of a fucosylated chondroitin sulfate. Thromb Haemost 100(3):420–428

    PubMed  CAS  Google Scholar 

  • Gomes AM, Kozlowski EO, Pomin VH, de Barros CM, Zaganeli JL, Pavao MS (2010) Unique extracellular matrix heparan sulfate from the bivalve nodipecten nodosus (Linnaeus, 1758) safely inhibits arterial thrombosis after photochemically induced endothelial lesion. J Biol Chem 285(10):7312–7323

    PubMed  CAS  Google Scholar 

  • Habuchi O, Sugiura K, Kawai N (1977) Glucose branches in chondroitin sulfates from squid cartilage. J Biol Chem 252(13):4570–4576

    PubMed  CAS  Google Scholar 

  • Habuchi O, Yamagata T, Suzuki S (1971) Biosynthesis of the acetylgalactosamine 4, 6-disulfate unit of squid chondroitin sulfate by transsulfation from 3′-phosphoadenosine 5′-phosphosulfate. J Biol Chem 246(23):7357–7365

    PubMed  CAS  Google Scholar 

  • Haefner B (2003) Drugs from the deep: marine natural products as drug candidates. Drug Discov Today 8(12):536–544

    PubMed  CAS  Google Scholar 

  • Helm MM, Bourne N (2004) The hatchery culture of bivalves: a practical manual Hatchery culture of bivalves. FAO, Rome

    Google Scholar 

  • Hikino M, Mikami T, Faissner A, Vilela-Silva AC, Pavao MS, Sugahara K (2003) Oversulfated dermatan sulfate exhibits neurite outgrowth-promoting activity toward embryonic mouse hippocampal neurons: implications of dermatan sulfate in neuritogenesis in the brain. J Biol Chem 278(44):43744–43754

    PubMed  CAS  Google Scholar 

  • Hirsh J, Warkentin TE, Shaughnessy SG, Anand SS, Halperin JL, Raschke R, Granger C, Ohman EM, Dalen JE (2001) Heparin and low-molecular-weight heparin: mechanisms of action, pharmacokinetics, dosing, monitoring, efficacy, and safety. Chest 119(1 Suppl):64S–94S

    PubMed  CAS  Google Scholar 

  • Hovingh P, Linker A (1982) An unusual heparan sulfate isolated from lobsters (homarus americanus). J Biol Chem 257(16):9840–9844

    PubMed  CAS  Google Scholar 

  • Jordan RE, Marcum JA (1986) Anticoagulantly active heparin from clam (mercenaria mercenaria). Arch Biochem Biophys 248(2):690–695

    PubMed  CAS  Google Scholar 

  • Karamanos NK (1992) Two squid skin proteoglycans each containing chondroitin sulfates with different sulfation patterns. Biochem Cell Biol 70(8):629–635

    PubMed  CAS  Google Scholar 

  • Karamanos NK, Aletras AJ, Antonopoulos CA, Hjerpe A (1994) Determination of the hnk-1 epitope (3-sulphated glucuronic acid) in intact chondroitin sulphates by ELISA. Application to squid skin proteoglycans and their oversulphated carbohydrate structures. Biochimie 76(1):79–82

    PubMed  CAS  Google Scholar 

  • Karamanos NK, Aletras AJ, Antonopoulos CA, Tsegenidis T, Tsiganos CP, Vynios DH (1988) Extraction and fractionation of proteoglycans from squid skin. Biochim Biophys Acta 966(1):36–43

    PubMed  CAS  Google Scholar 

  • Karamanos NK, Manouras A, Tsegenidis T, Antonopoulos CA (1991) Isolation and chemical study of the glycosaminoglycans from squid cornea. Int J Biochem 23(1):67–72

    PubMed  CAS  Google Scholar 

  • Kariya Y, Sakai T, Kaneko T, Suzuki K, Kyogashima M (2002) Enhancement of t-pa-mediated plasminogen activation by partially defucosylated glycosaminoglycans from the sea cucumber Stichopus japonicus. J Biochem 132(2):335–343

    PubMed  CAS  Google Scholar 

  • Kariya Y, Watabe S, Hashimoto K, Yoshida K (1990) Occurrence of chondroitin sulfate e in glycosaminoglycan isolated from the body wall of sea cucumber Stichopus japonicus. J Biol Chem 265(9):5081–5085

    PubMed  CAS  Google Scholar 

  • Kariya Y, Watabe S, Kyogashima M, Ishihara M, Ishii T (1997) Structure of fucose branches in the glycosaminoglycan from the body wall of the sea cucumber Stichopus japonicus. Carbohydr Res 297(3):273–279

    PubMed  CAS  Google Scholar 

  • Kawai Y, Seno N, Anno K (1966) Chondroitin polysulfate of squid cartilage. J Biochem 60(3):317–321

    PubMed  CAS  Google Scholar 

  • Kawashima H, Atarashi K, Hirose M, Hirose J, Yamada S, Sugahara K, Miyasaka M (2002) Oversulfated chondroitin/dermatan sulfates containing glcabeta1/idoaalpha1–3galnac(4, 6-o-disulfate) interact with l- and p-selectin and chemokines. J Biol Chem 277(15):12921–12930

    PubMed  CAS  Google Scholar 

  • Kinoshita A, Yamada S, Haslam SM, Morris HR, Dell A, Sugahara K (1997) Novel tetrasaccharides isolated from squid cartilage chondroitin sulfate e contain unusual sulfated disaccharide units glca(3-o-sulfate)beta1-3galnac(6-o-sulfate) or glca(3-o-sulfate)beta1-3galnac. J Biol Chem 272(32):19656–19665

    PubMed  CAS  Google Scholar 

  • Kinoshita-Toyoda A, Yamada S, Haslam SM, Khoo KH, Sugiura M, Morris HR, Dell A, Sugahara K (2004) Structural determination of five novel tetrasaccharides containing 3-o-sulfated d-glucuronic acid and two rare oligosaccharides containing a beta-d-glucose branch isolated from squid cartilage chondroitin sulfate e. Biochemistry 43(34):11063–11074

    PubMed  CAS  Google Scholar 

  • Lem A (2005) International trade in aquaculture products. Topics fact sheets. Department FFaA, Rome

    Google Scholar 

  • Lindahl U, Backstrom G, Thunberg L, Leder IG (1980) Evidence for a 3-o-sulfated d-glucosamine residue in the antithrombin-binding sequence of heparin. Proc Natl Acad Sci USA 77(11):6551–6555

    PubMed  CAS  Google Scholar 

  • Linhardt RJ, Ampofo SA, Fareed J, Hoppensteadt D, Mulliken JB, Folkman J (1992) Isolation and characterization of human heparin. Biochemistry 31(49):12441–12445

    PubMed  CAS  Google Scholar 

  • Liu H, Zhang Z, Linhardt RJ (2009) Lessons learned from the contamination of heparin. Nat Prod Rep 26(3):313–321

    PubMed  CAS  Google Scholar 

  • Luppi E, Cesaretti M, Volpi N (2005) Purification and characterization of heparin from the Italian clam callista chione. Biomacromolecules 6(3):1672–1678

    PubMed  CAS  Google Scholar 

  • Martin JG, Gupta M, Xu Y, Akella S, Liu J, Dordick JS, Linhardt RJ (2009) Toward an artificial golgi: redesigning the biological activities of heparan sulfate on a digital microfluidic chip. J Am Chem Soc 131(31):11041–11048

    PubMed  CAS  Google Scholar 

  • Mathews MB, Duh J, Person P (1962) Acid mucopolysaccharides of invertebrate cartilage. Nature 193:378–379

    PubMed  CAS  Google Scholar 

  • Medeiros GF, Mendes A, Castro RA, Bau EC, Nader HB, Dietrich CP (2000) Distribution of sulfated glycosaminoglycans in the animal kingdom: widespread occurrence of heparin-like compounds in invertebrates. Biochim Biophys Acta 1475(3):287–294

    PubMed  CAS  Google Scholar 

  • Molinski T (2009) Marine natural products. Clin Adv Hematol Oncol 7(6):383–385

    PubMed  Google Scholar 

  • Mourao PA, Boisson-Vidal C, Tapon-Bretaudiere J, Drouet B, Bros A, Fischer A (2001) Inactivation of thrombin by a fucosylated chondroitin sulfate from echinoderm. Thromb Res 102(2):167–176

    PubMed  CAS  Google Scholar 

  • Mourao PA, Pavao MS, Mulloy B, Wait R (1997) Chondroitin abc lyase digestion of an ascidian dermatan sulfate. Occurrence of unusual 6-o-sulfo-2-acetamido-2-deoxy-3-o-(2-o-sulfo-alpha-l-idopyranosyluronic acid)-beta-d-galactose units. Carbohydr Res 300(4):315–321

    PubMed  CAS  Google Scholar 

  • Mourao PA, Pereira MS, Pavao MS, Mulloy B, Tollefsen DM, Mowinckel MC, Abildgaard U (1996) Structure and anticoagulant activity of a fucosylated chondroitin sulfate from echinoderm. Sulfated fucose branches on the polysaccharide account for its high anticoagulant action. J Biol Chem 271(39):23973–23984

    PubMed  CAS  Google Scholar 

  • Nader HB, Ferreira TM, Paiva JF, Medeiros MG, Jeronimo SM, Paiva VM, Dietrich CP (1984) Isolation and structural studies of heparan sulfates and chondroitin sulfates from three species of molluscs. J Biol Chem 259(3):1431–1435

    PubMed  CAS  Google Scholar 

  • Nader HB, Pinhal MA, Bau EC, Castro RA, Medeiros GF, Chavante SF, Leite EL, Trindade ES, Shinjo SK, Rocha HA, Tersariol IL, Mendes A, Dietrich CP (2001) Development of new heparin-like compounds and other antithrombotic drugs and their interaction with vascular endothelial cells. Braz J Med Biol Res 34(6):699–709

    PubMed  CAS  Google Scholar 

  • Nandini CD, Mikami T, Ohta M, Itoh N, Akiyama-Nambu F, Sugahara K (2004) Structural and functional characterization of oversulfated chondroitin sulfate/dermatan sulfate hybrid chains from the notochord of hagfish. Neuritogenic and binding activities for growth factors and neurotrophic factors. J Biol Chem 279(49):50799–50809

    PubMed  CAS  Google Scholar 

  • Nobuko S, Murakami K (1982) Structure of disulfated disaccharides from chondroitin polysulfates, chondroitin sulfate d and k. Carbohydr Res 103(1):190–194

    Google Scholar 

  • Oguri K, Yamagata T (1978) Appearance of a proteoglycan in developing sea urchin embryos. Biochim Biophys Acta 541(3):385–393. doi:0304-4165(78)90197-6 [pii]

    PubMed  CAS  Google Scholar 

  • Pavao MS, Aiello KR, Werneck CC, Silva LC, Valente AP, Mulloy B, Colwell NS, Tollefsen DM, Mourao PA (1998) Highly sulfated dermatan sulfates from ascidians. Structure versus anticoagulant activity of these glycosaminoglycans. J Biol Chem 273(43):27848–27857

    PubMed  CAS  Google Scholar 

  • Pavao MS, Mourao PA, Mulloy B, Tollefsen DM (1995) A unique dermatan sulfate-like glycosaminoglycan from ascidian. Its structure and the effect of its unusual sulfation pattern on anticoagulant activity. J Biol Chem 270(52):31027–31036

    PubMed  CAS  Google Scholar 

  • Pavao MS, Rodrigues MA, Mourao PA (1994) Acidic polysaccharides of the ascidian styela plicata. Biosynthetic studies on the sulfated l-galactans of the tunic, and preliminary characterization of a dermatan sulfate-like polymer in body tissues. Biochim Biophys Acta 1199(3):229–237

    PubMed  CAS  Google Scholar 

  • Pejler G, Danielsson A, Bjork I, Lindahl U, Nader HB, Dietrich CP (1987) Structure and antithrombin-binding properties of heparin isolated from the clams anomalocardia brasiliana and tivela mactroides. J Biol Chem 262(24):11413–11421

    PubMed  CAS  Google Scholar 

  • Pomin VH (2009) Review: an overview about the structure-function relationship of marine sulfated homopolysaccharides with regular chemical structures. Biopolymers 91(8):601–609

    PubMed  CAS  Google Scholar 

  • Pomin VH, Mourao PA (2008) Structure, biology, evolution, and medical importance of sulfated fucans and galactans. Glycobiology 18(12):1016–1027

    PubMed  CAS  Google Scholar 

  • Roden L, Ananth S, Campbell P, Curenton T, Ekborg G, Manzella S, Pillion D, Meezan E (1992) Heparin – an introduction. Adv Exp Med Biol 313:1–20

    PubMed  CAS  Google Scholar 

  • Santos EA, Rocha LR, Pereira NM, Andrade GP, Nader HB, Dietrich CP (2002) Mast cells are present in epithelial layers of different tissues of the mollusc anomalocardia brasiliana. In situ characterization of heparin and a correlation of heparin and histamine concentration. Histochem J 34(11–12):553–558

    PubMed  CAS  Google Scholar 

  • Santos JC, Mesquita JM, Belmiro CL, da Silveira CB, Viskov C, Mourier PA, Pavao MS (2007) Isolation and characterization of a heparin with low antithrombin activity from the body of styela plicata (chordata-tunicata). Distinct effects on venous and arterial models of thrombosis. Thromb Res 121(2):213–223

    PubMed  CAS  Google Scholar 

  • Saravanan R, Shanmugam A (2010a) Isolation and characterization of low molecular weight glycosaminoglycans from marine mollusc amussium pleuronectus (linne) using chromatography. Appl Biochem Biotechnol 160(3):791–799

    PubMed  CAS  Google Scholar 

  • Saravanan R, Shanmugam A (2010b) Preventive effect of low molecular weight glycosaminoglycan from amussium pleuronectus (linne) on oxidative injury and cellular abnormalities in isoproterenol-induced cardiotoxicity in wistar rats. Appl Biochem Biotechnol 162(1):43–51

    PubMed  CAS  Google Scholar 

  • Seeberger PH, Werz DB (2007) Synthesis and medical applications of oligosaccharides. Nature 446(7139):1046–1051

    PubMed  CAS  Google Scholar 

  • Shetty AK, Kobayashi T, Mizumoto S, Narumi M, Kudo Y, Yamada S, Sugahara K (2009) Isolation and characterization of a novel chondroitin sulfate from squid liver integument rich in n-acetylgalactosamine(4, 6-disulfate) and glucuronate(3-sulfate) residues. Carbohydr Res 344(12):1526–1532

    PubMed  CAS  Google Scholar 

  • Sugahara K, Tanaka Y, Yamada S, Seno N, Kitagawa H, Haslam SM, Morris HR, Dell A (1996) Novel sulfated oligosaccharides containing 3-o-sulfated glucuronic acid from king crab cartilage chondroitin sulfate k. Unexpected degradation by chondroitinase abc. J Biol Chem 271(43):26745–26754

    PubMed  CAS  Google Scholar 

  • Tamura J, Arima K, Imazu A, Tsutsumishita N, Fujita H, Yamane M, Matsumi Y (2009) Sulfation patterns and the amounts of chondroitin sulfate in the diamond squid, Thysanoteuthis rhombus. Biosci Biotechnol Biochem 73(6):1387–1391

    PubMed  CAS  Google Scholar 

  • Tapon-Bretaudiere J, Drouet B, Matou S, Mourao PA, Bros A, Letourneur D, Fischer AM (2000) Modulation of vascular human endothelial and rat smooth muscle cell growth by a fucosylated chondroitin sulfate from echinoderm. Thromb Haemost 84(2):332–337

    PubMed  CAS  Google Scholar 

  • Ueoka C, Kaneda N, Okazaki I, Nadanaka S, Muramatsu T, Sugahara K (2000) Neuronal cell adhesion, mediated by the heparin-binding neuroregulatory factor midkine, is specifically inhibited by chondroitin sulfate e. Structural and functional implications of the over-sulfated chondroitin sulfate. J Biol Chem 275(48):37407–37413

    PubMed  CAS  Google Scholar 

  • Ulrich PN, Boon JK (2001) The histological localization of heparin in the northern quahog clam, mercenaria mercenaria. J Invertebr Pathol 78(3):155–159

    PubMed  CAS  Google Scholar 

  • Vicente CP, He L, Pavao MS, Tollefsen DM (2004) Antithrombotic activity of dermatan sulfate in heparin cofactor II-deficient mice. Blood 104(13):3965–3970

    PubMed  CAS  Google Scholar 

  • Vicente CP, Zancan P, Peixoto LL, Alves-Sa R, Araujo FS, Mourao PA, Pavao MS (2001) Unbalanced effects of dermatan sulfates with different sulfation patterns on coagulation, thrombosis and bleeding. Thromb Haemost 86(5):1215–1220

    PubMed  CAS  Google Scholar 

  • Vieira RP, Mourao PA (1988) Occurrence of a unique fucose-branched chondroitin sulfate in the body wall of a sea cucumber. J Biol Chem 263(34):18176–18183

    PubMed  CAS  Google Scholar 

  • Vieira RP, Mulloy B, Mourao PA (1991) Structure of a fucose-branched chondroitin sulfate from sea cucumber. Evidence for the presence of 3-o-sulfo-beta-d-glucuronosyl residues. J Biol Chem 266(21):13530–13536

    PubMed  CAS  Google Scholar 

  • Vijayabaskar P, Balasubramanian T, Somasundaram ST (2008) Low-molecular weight molluscan glycosaminoglycan from bivalve katelysia opima (gmelin). Methods Find Exp Clin Pharmacol 30(3):175–180

    PubMed  CAS  Google Scholar 

  • Vijayabaskar P, Somasundaram ST (2009) Histological localization and analytical evaluation of heparin in the wedge clam donax cuneatus (linnaeus, 1758). Method Find Exp Clin 31(5):311–316

    CAS  Google Scholar 

  • Vilela-Silva AC, Werneck CC, Valente AP, Vacquier VD, Mourao PA (2001) Embryos of the sea urchin strongylocentrotus purpuratus synthesize a dermatan sulfate enriched in 4-o- and 6-o-disulfated galactosamine units. Glycobiology 11(6):433–440

    PubMed  CAS  Google Scholar 

  • Volpi N, Maccari F (2009) Structural characterization and antithrombin activity of dermatan sulfate purified from marine clam scapharca inaequivalvis. Glycobiology 19(4):356–367

    PubMed  CAS  Google Scholar 

  • Wang L, Brown JR, Varki A, Esko JD (2002) Heparin’s anti-inflammatory effects require glucosamine 6-o-sulfation and are mediated by blockade of l- and p-selectins. J Clin Invest 110(1):127–136

    PubMed  CAS  Google Scholar 

  • Xu CX, Jin H, Chung YS, Shin JY, Lee KH, Beck GR Jr, Palmos GN, Choi BD, Cho MH (2008a) Chondroitin sulfate extracted from ascidian tunic inhibits phorbol ester-induced expression of inflammatory factors vcam-1 and cox-2 by blocking nf-kappab activation in mouse skin. J Agric Food Chem 56(20):9667–9675

    PubMed  CAS  Google Scholar 

  • Xu CX, Jin H, Chung YS, Shin JY, Woo MA, Lee KH, Palmos GN, Choi BD, Cho MH (2008b) Chondroitin sulfate extracted from the styela clava tunic suppresses tnf-alpha-induced expression of inflammatory factors, vcam-1 and inos by blocking akt/nf-kappab signal in jb6 cells. Cancer Lett 264(1):93–100

    PubMed  CAS  Google Scholar 

  • Yamada S, Morimoto H, Fujisawa T, Sugahara K (2007) Glycosaminoglycans in hydra magnipapillata (hydrozoa, cnidaria): demonstration of chondroitin in the developing nematocyst, the sting organelle, and structural characterization of glycosaminoglycans. Glycobiology 17(8):886–894

    PubMed  CAS  Google Scholar 

  • Yamaguchi M, Kinoshita S, Suzuki N (1989) Dermatan sulfate formation in gastrulae of the sea urchin Clypeaster japonicus. J Biochem 106(1):158–162

    PubMed  CAS  Google Scholar 

  • Zancan P, Mourao PA (2004) Venous and arterial thrombosis in rat models: dissociation of the antithrombotic effects of glycosaminoglycans. Blood Coagul Fibrinolysis 15(1):45–54

    PubMed  CAS  Google Scholar 

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Acknowledgments

The work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Mizutani Foundation for Glycoscience (to MSGP); MSGP is a research fellow from FAPERJ and CNPq.

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Authors and Affiliations

  1. Programa de Glicobiologia, Instituto de Bioquímica Médica and Hospital Universitário Clementino Fraga Filho, Universidade Federal do Rio de Janeiro, Cidade Universitaria, Rio de Janeiro, Brazil

    Eliene O. Kozlowski, Angélica M. Gomes, Christiane Sobral Silva & Mauro S. G. Pavão

  2. Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Centro de Ciências da Saúde, Cidade Universitaria, Rio de Janeiro, Brazil

    Mariana Sá Pereira & Ana Cristina E. S. de Vilela Silva

  3. Laboratório de Tecido Conjuntivo, Hospital Universitário Clementino Fraga Filho, Cidade Universitária, Rua Rodolpho Paulo Rocco 255, 4° andar, sala 4A-08, CEP 21941-913, Rio de Janeiro, Brazil

    Mauro S. G. Pavão

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  1. Eliene O. Kozlowski
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  2. Angélica M. Gomes
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  3. Christiane Sobral Silva
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  4. Mariana Sá Pereira
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  5. Ana Cristina E. S. de Vilela Silva
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  6. Mauro S. G. Pavão
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Correspondence to Mauro S. G. Pavão .

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  1. , Institute of Medical Biochemistry, Federal University of Rio de Janeiro, Av. Prof. Rodolpho Paulo Rocco 255, Rio de Janeiro, 21941-913, Rio de Janeiro, Brazil

    Mauro S.G. Pavão

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Kozlowski, E.O., Gomes, A.M., Silva, C.S., Pereira, M.S., de Vilela Silva, A.C.E.S., Pavão, M.S.G. (2011). Structure and Biological Activities of Glycosaminoglycan Analogs from Marine Invertebrates: New Therapeutic Agents?. In: Pavão, M. (eds) Glycans in Diseases and Therapeutics. Biology of Extracellular Matrix. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-16833-8_7

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