Applications of Glycosaminoglycans in the Medical, Veterinary, Pharmaceutical, and Cosmetic Fields

Chapter

Abstract

Glycosaminoglycans (GAGs) are complex polysaccharides ubiquitously present in the extracellular matrix of mammalian tissues, where they constitute the gelatinous material responsible for maintaining the cells together, in an intimate association with a variety of proteins. Although their structures are not strictly regular, they are composed of a repeating unit of a hexosamine-containing disaccharide. Most of them possess uronic acid residues, and with the exception of hyaluronic acid, they also carry sulfate groups. As a consequence of their high negative charge, they have an extraordinary capacity to absorb water. GAGs participate in many relevant biological processes by interaction with a plethora of proteins, and thus, a large number of applications in different fields have been conceived for GAGs and their derivatives.

Keywords

Glycosaminoglycan Sulfation Alzheimer’s disease Tissue engineering Cancer treatment Osteoarthritis Skin hydration Cross-linked glycosaminoglycans 

References

  1. Afratis NA, Gialeli C, Nikitovic D, Tsegenidis T, Karousou E, Theocharis AD, Pavao MS, Tzanakakis GN, Karamanos NK (2012) Glycosaminoglycans: key players in cancer cell biology and treatment. FEBS J 279:1177–1197CrossRefGoogle Scholar
  2. Afratis NA, Karamanos NK, Piperigkou Z, Vynios DH, Theocharis AD (2016) The role of heparins and nano-heparins as therapeutic tool in breast cancer. Glycoconj J. 2016. doi: 10.1007/s10719-016-9742-7
  3. Ahmad S, Ansari AA (2011) Therapeutic roles of heparin anticoagulants in cancer and related disorders. Med Chem 7:504–517CrossRefGoogle Scholar
  4. Aimi T, Suzuki K, Hoshino T, Mizushima T (2015) Dextran sulfate sodium inhibits amyloid-β oligomer binding to cellular prion protein. J Neurochem 134:611–617CrossRefGoogle Scholar
  5. Aquino SA, Park PW (2010) Diverse functions of glycosaminoglycans in infectious diseases. Prog Mol Biol Transl Sci 93:373–394CrossRefGoogle Scholar
  6. Aquino SA, Park PW (2016) Glycosaminoglycans and infection. Front Biosci (Landmark Ed) 21:1260–1277CrossRefGoogle Scholar
  7. Arevalo MT, Simpson-Haidaris PJ, Jin X, Chen H, Quinn MH (2011) Compositions and methods for inhibition of or treatment of dengue virus infection. PCT Int Appl WO 2011153458Google Scholar
  8. Axelsson J, Xu D, Kang BN, Nussbacher JK, Handel TM, Ley K, Sriramarao P, Esko JD (2012) Inactivation of heparan sulfate 2-O-sulfotransferase accentuates neutrophil infiltration during acute inflammation in mice. Blood 120:1742–1751CrossRefGoogle Scholar
  9. Bachar G, Cohen K, Hod R, Feinmesser R, Mizrachi A, Shpitzer T, Katz O, Peer D (2011) Hyaluronan-grafted particle clusters loaded with mitomycin C as selective nanovectors for primary head and neck cancers. Biomaterials 32:4840–4848CrossRefGoogle Scholar
  10. Badylak SF (1997) Biomaterial derived from vertebrate liver tissue. US Patent 6,379,710Google Scholar
  11. Badylak SF, Demeter RJ, Hiles M, Voytik SL, Knapp PM Jr (1994) Fluidized intestinal submucosa and its use as an injectable tissue graft. US Patent 5,275,826 AGoogle Scholar
  12. Badylak SF, Voytik SL, Brightman A, Waninger M (1995) Urinary bladder submucosa derived tissue graft. US Patent 5,554,389Google Scholar
  13. Badylak SF, Voytik-Harbin SL, Brightman AO, Tullius RS (1997) Stomach submucosa derived tissue graft. US Patent 6,099,567Google Scholar
  14. Barrowcliffe TJ (2012) History of heparin. Handb Exp Pharmacol 207:3–22CrossRefGoogle Scholar
  15. Basappa, Rangappa KS, Sugahara K (2014) Roles of glycosaminoglycans and glycanmimetics in tumor progression and metastasis. Glycoconj J 31:461–467CrossRefGoogle Scholar
  16. Beasley KL, Weiss M, Weiss RA (2009) Hyaluronic acid fillers: a comprehensive review. Facial Plast Surg 25:86–94CrossRefGoogle Scholar
  17. Bedini E, Parrilli M (2012) Synthetic and semi-synthetic chondroitin sulfate oligosaccharides, polysaccharides, and glycomimetics. Carbohydr Res 356:75–85CrossRefGoogle Scholar
  18. Belting M (2014) Glycosaminoglycans in cancer treatment. Thromb Res 133:S95–S101CrossRefGoogle Scholar
  19. Benitez A, Yates TJ, Lopez LE, Cerwinka WH, Bakkar A, Lokeshwar VB (2011) Targeting hyaluronidase for cancer therapy: antitumor activity of sulfated hyaluronic acid in prostate cancer cells. Cancer Res 71:4085–4095CrossRefGoogle Scholar
  20. Bernstein EF, Underhill CB, Hahn PJ, Brown DB, Uitto J (1996) Chronic sun exposure alters both the content and distribution of dermal glycosaminoglycans. Br J Dermatol 135:255–262CrossRefGoogle Scholar
  21. Boeriu CG, Springer J, Kooy FK, van den Broek LAM, Eggink G (2013) Production methods for hyaluronan. Int J Carbohydr Chem. Article ID 624967 2013:14CrossRefGoogle Scholar
  22. Bonafe F, Govoni M, Giordano E, Caldarera C, Guarnieri C, Muscari C (2014) Hyaluronan and cardiac regeneration. J Biomed Sci 21:100. 13 ppCrossRefGoogle Scholar
  23. Borsig L, Vlodavsky I, Ishai-Michaeli R, Torri G, Vismara E (2011) Sulfated hexasaccharides attenuate metastasis by inhibition of P-selectin and heparanase. Neoplasia 13:445–452CrossRefGoogle Scholar
  24. Bottegoni C, Muzzarelli RAA, Giovannini F, Busilacchi A, Gigante A (2014) Oral chondroprotection with nutraceuticals made of chondroitin sulphate plus glucosamine sulphate in osteoarthritis. Carbohydr Polym 109:126–138CrossRefGoogle Scholar
  25. Brougham CM, Levingstone TJ, Jockenhoevel S, Flanagan TC, O’Brien FJ (2015) Incorporation of fibrin into a collagen–glycosaminoglycan matrix results in a scaffold with improved mechanical properties and enhanced capacity to resist cell-mediated contraction. Acta Biomater 26:205–214CrossRefGoogle Scholar
  26. Cagno V, Donalisio M, Civra A, Volante M, Veccelli E, Oreste P, Rusnati M, Lembo D (2014) Highly sulfated K5 Escherichia coli polysaccharide derivatives inhibit respiratory syncytial virus infectivity in cell lines and human tracheal-bronchial histocultures. Antimicrob Agents Chemother 58:4782–4794CrossRefGoogle Scholar
  27. Campion C, Pini APJ, Gogoi RN, Gilthorpe J (2012) Sulfated oligosaccharides for use in treatment of neurodegenerative diseases. PCT Int Appl WO 2012/160337Google Scholar
  28. Capila I, Linhardt RJ (2002) Heparin-protein interactions. Angew Chem Int Ed Eng 41:390–412CrossRefGoogle Scholar
  29. Cayre Y, Allouche R (2017) Produit pour lutter contre la prolifération des cellules cancéreuse. Fr Demande FR 3039065Google Scholar
  30. Chang P-h (2014) Pharmaceutical formulation containing glycosaminoglycan. PCT Int Appl WO 2014142938, PCT Int Appl WO 2014143085Google Scholar
  31. Cheng G, Cao B (2015) Zwitterionic polysaccharide polymers having antifouling, antimicrobial and optical transparency properties. PCT Int Appl WO 2015057645 A1Google Scholar
  32. Conrad HE (ed) (1998) Heparin-binding proteins. Academic, San DiegoGoogle Scholar
  33. Coombe DR, Kett WC (2005) Heparan sulfate-protein interactions: therapeutic potential through structure-function insights. Cell Mol Life Sci 62:410–424CrossRefGoogle Scholar
  34. Coppa GV, Facinelli B, Magi G, Marini E, Zampini L, Mantovani V, Galeazzi T, Padella L, Marchesiello RL, Santoro L, Coscia A, Peila C, Volpi N, Gabrielli O (2016) Human milk glycosaminoglycans inhibit in vitro the adhesion of Escherichia coli and Salmonella fyris to human intestinal cells. Pediatr Res 79:603–607CrossRefGoogle Scholar
  35. Cordo Russo RI, García MG, Alaniz L, Blanco G, Alvarez E, Hajos SE (2008) Hyaluronan oligosaccharides sensitize lymphoma resistant cell lines to vincristine by modulating P-glycoprotein activity and PI3K/Akt pathway. Int J Cancer 122:1012–1018CrossRefGoogle Scholar
  36. Crepaldi G, Fellin R, Calabrò A, Rossi A, Ventura A, Mannarino E, Senin U, Ciuffetti G, Descovich GC, Gaddi A, Rimondi S, Pozza G, Vicari A, Carandente O, Mancini M, Rubba P, Postiglione A, Strano A, Avellone G, Davì G, Novo S, Pinto A, Capurso A, Resta F, Mogavero AM, Bucci A, Antonini R, Lalloni L (1990) Double-blind multicenter trial on a new medium molecular weight glycosaminoglycan current therapeutic effects and perspectives for clinical use. Atherosclerosis 81:233–243CrossRefGoogle Scholar
  37. Cruz L, Meyers C (2013) Differential dependence on host cell glycosaminoglycans for infection of epithelial cells by high-risk HPV types. PLoS One 8:e68379CrossRefGoogle Scholar
  38. Da Costa Dias B, Jovanovic K, Gonsalves D, Weiss SFT (2011) Structural and mechanistic commonalities of amyloid-β and the prion protein. Prion 5:126–137CrossRefGoogle Scholar
  39. Davis DAS, Parish CR (2013) Heparan sulfate: a ubiquitous glycosaminoglycan with multiple roles in immunity. Front Immunol 4:470. 7 ppGoogle Scholar
  40. De Vita D, Giordano S (2012) Effectiveness of intravesical hyaluronic acid/chondroitin sulfate in recurrent bacterial cystitis: a randomized study. Int Urogynecol J 23:1707–1713CrossRefGoogle Scholar
  41. DeAngelis PL, Lane RS (2016) Heparosan/therapeutic prodrug complexes and methods of making and using same. WO 2016/065309Google Scholar
  42. DeAngelis PL, Liu J, Linhardt RJ (2013) Chemoenzymatic synthesis of glycosaminoglycans: re-creating, re-modeling and re-designing nature’s longest or most complex carbohydrate chains. Glycobiology 23:764–777CrossRefGoogle Scholar
  43. Della Valle F, Romeo A (1989) Esters of hyaluronic acid. US Patent 4,851,521Google Scholar
  44. Dicker KT, Gurski LA, Pradhan-Bhatt S, Witt RL, Farach-Carson MC, Jia X (2014) Hyaluronan: a simple polysaccharide with diverse biological functions. Acta Biomater 10:1558–1570CrossRefGoogle Scholar
  45. Eklund E, Ekman-Ordeberg G, Malmstrom A (2013) Treatment of cytokine mediated conditions. Can Pat Appl CA 2779838Google Scholar
  46. Esko JD (2001) Special considerations for proteoglycans and glycosaminoglycans and their purification. Curr Protoc Mol Biol 17:17.2.1–17.2.9Google Scholar
  47. Fabricius H-A (2015) Sulfated polysaccharides for use in the treatment of cancer. PCT Int Appl WO 2015/059177Google Scholar
  48. Finelli I, Chiessi E, Galesso D, Renier D, Paradossi G (2009) Gel-like structure of a hexadecyl derivative of hyaluronic acid for the treatment of osteoarthritis. Macromol Biosci 9:646–653CrossRefGoogle Scholar
  49. Fitton H, Gardiner V (2011) Anti-viral formulations. PCT Int Appl WO 2011/100805Google Scholar
  50. Flores Salgado F, Benitez Jimenez AF, Costa Rierola M, Flores Costa R, Flores Costa L (2013) Partially depolymerized glycosaminoglycan silver and gold salts. PCT Int Appl WO 2013/121001Google Scholar
  51. Freudenberg U, Zieris A, Chwalek K, Tsurkan MV, Maitz MF, Atallah P, Levental KR, Eming SA, Werner C (2015) Heparin desulfation modulates VEGF release and angiogenesis in diabetic wounds. J Control Release 220(Part A):79–88CrossRefGoogle Scholar
  52. Fu L, Suflita M, Linhardt RJ (2016) Bioengineered heparins and heparan sulfates. Adv Drug Deliv Rev 97:237–249CrossRefGoogle Scholar
  53. Fukuda T, Matsumoto E, Miura Y (2015) Interaction between multimeric sulfated saccharides and Alzheimer amyloid β (1-42). Chem Lett 44:1482–1484CrossRefGoogle Scholar
  54. Funderburgh JL (2000) Keratan sulfate: structure, biosynthesis, and function. Glycobiology 10:951–958CrossRefGoogle Scholar
  55. Fux L, Ilan N, Sanderson RD, Vlodavsky I (2009) Heparanase: busy at the cell surface. Trends Biochem Sci 34:511–519CrossRefGoogle Scholar
  56. Galus A, Mallet J-M, Lembo D, Cagno V, Djabourov M, Lortat-Jacob H, Bouchemal K (2016) Hexagonal-shaped chondroitin sulfate self-assemblies have exalted anti-HSV-2 activity. Carbohydr Polym 136:113–120CrossRefGoogle Scholar
  57. García B, Merayo-Lloves J, Martin C, Alcalde I, Quirós LM, Vazquez F (2016) Surface proteoglycans as mediators in bacterial pathogens infections. Front Microbiol 7:220. 11 ppGoogle Scholar
  58. Genco T, Zemljič LF, Bračič M, Stana-Kleinschek K, Heinze T (2012) Physicochemical properties and bioactivity of a novel class of cellulosics: 6-deoxy-6-amino cellulose sulfate. Macromol Chem Phys 213:539–548CrossRefGoogle Scholar
  59. Gilbert TW, Sellaro TL, Badylak SF (2006) Decellularization of tissues and organs. Biomaterials 27:3675–3683Google Scholar
  60. Gomes AM, Stelling MP, Pavão MSG (2013, 2013) Heparan sulfate and heparanase as modulators of breast cancer progression. BioMed Res Int:852093. 11 ppGoogle Scholar
  61. Gomes AM, Kozlowski EO, Borsig L, Teixeira FCOB, Vlodavsky I, Pavão MSG (2015) Antitumor properties of a new non-anticoagulant heparin analog from the mollusk Nodipecten nodosus: effect on P-selectin, heparanase, metastasis and cellular recruitment. Glycobiology 25:386–393CrossRefGoogle Scholar
  62. Gray E, Hogwood J, Mulloy B (2012) The anticoagulant and antithrombotic mechanisms of heparin. Handb Exp Pharmacol 207:43–61CrossRefGoogle Scholar
  63. Grohmann S, Hildebrand G, Liefeith K (2014) Active substance-loaded biocompatible polyelectrolyte multilayers based on sulfated glycosaminoglycans, methods for producing the multilayers, and use of the multilayers. PCT Int Appl WO 2014/147080; Ger Offen DE 102013204742Google Scholar
  64. Harenberg J (1998) Review of pharmacodynamics, pharmacokinetics, and therapeutic properties of sulodexide. Med Res Rev 18:1–20CrossRefGoogle Scholar
  65. Hendricks GL, Velazquez L, Pham S, Qaisar N, Delaney JC, Viswanathan K, Albers L, Comolli JC, Shriver Z, Knipe DM, Kurt-Jones EA, Fygenson DK, Trevejo JM, Wang JP, Finberg RW (2015) Heparin octasaccharide decoy liposomes inhibit replication of multiple viruses. Antivir Res 116:34–44CrossRefGoogle Scholar
  66. Herrero LJ, Foo S-S, Sheng K-C, Chen W, Forwood MR, Bucala R, Mahalingam S (2015) Pentosan polysulfate: a novel glycosaminoglycan-like molecule for the effective treatment of alphavirus-induced cartilage destruction and inflammatory disease. J Virol 89:8063–8076CrossRefGoogle Scholar
  67. Herrero-Mendez A, Palomares T, Castro B, Herrero J, Granado MH, Bejar JM, Alonso-Varona A (2015) HR007: a family of biomaterials based on glycosaminoglycans for tissue repair. J Tissue Eng Regen Med. doi: 10.1002/term.1998
  68. Hidari KI, Abe T, Suzuki T (2013) Carbohydrate-related inhibitors of dengue virus entry. Viruses 5:605–618CrossRefGoogle Scholar
  69. Hoshiba T, Chen G, Endo C, Maruyama H, Wakui M, Nemoto E, Kawazoe N, Tanaka M (2016) Decellularized extracellular matrix as an in vitro model to study the comprehensive roles of the ECM in stem cell differentiation. Stem Cells Int. Article ID 6397820, 10 ppGoogle Scholar
  70. Huang Y, Yao X, Zhang R, Ouyang L, Jiang R, Liu X, Song C, Zhang G, Fan Q, Wang L, Huang W (2014) Cationic conjugated polymer/fluoresceinamine-hyaluronan complex for sensitive fluorescence detection of CD44 and tumor-targeted cell imaging. ACS Appl Mater Interfaces 6:19144–19153CrossRefGoogle Scholar
  71. Jia X, Kiick KL (2009) Hybrid multicomponent hydrogels for tissue engineering. Macromol Biosci 9:140–156CrossRefGoogle Scholar
  72. Jinno-Oue A, Tanaka A, Shimizu N, Mori T, Sugiura N, Kimata K, Isomura H, Hoshino H (2013) Inhibitory effect of chondroitin sulfate type E on the binding step of human T-cell leukemia virus type 1. AIDS Res Hum Retrovir 29:621–629CrossRefGoogle Scholar
  73. Kallestrup E, Jørgensen S, Nordling J, Hald T (2005) Treatment of interstitial cystitis with Cystistat®, a hyaluronic acid product. Scand J Urol Nephrol 39:143–147CrossRefGoogle Scholar
  74. Kavasi RM, Berdiaki A, Spyridaki I, Corsini E, Tsatsakis A, Tzanakakis G, Nikitovic D (2017) HA metabolism in skin homeostasis and inflammatory disease. Food Chem Toxicol 101:128–138CrossRefGoogle Scholar
  75. Keane TJ, Swinehart IT, Badylak SF (2015) Methods of tissue decellularization used for preparation of biologic scaffolds and in vivo relevance. Methods 84:25–34CrossRefGoogle Scholar
  76. Khaderi K (2014) Compositions and methods for treating injuries to the visual system of a human. US Patent 0,212,404 A1Google Scholar
  77. Khanlari A, Detamore MS, Gehrke SH (2013) Increasing cross-linking efficiency of methacrylated chondroitin sulfate hydrogels by copolymerization with oligo(ethylene glycol) diacrylates. Macromolecules 46:9609–9617CrossRefGoogle Scholar
  78. Khanlari A, Suekama TC, Gehrke SH (2015a) Structurally versatile glycosaminoglycan hydrogels for biomedical applications. Macromol Symp 358:67–77CrossRefGoogle Scholar
  79. Khanlari A, Suekama TC, Detamore MS, Gehrke SH (2015b) Structurally diverse and readily tunable photocrosslinked chondroitin sulfate based copolymers. J Polym Sci Part B Polym Phys 53:1070–1079CrossRefGoogle Scholar
  80. Khanlari A, Schulteis JE, Suekama TC, Detamore MS, Gehrke SH (2015c) Designing crosslinked hyaluronic acid hydrogels with tunable mechanical properties for biomedical applications. J Appl Polym Sci 132. doi: 10.1002/APP.42009
  81. Kim E, Okumura M, Sawa H, Miyazaki T, Fujikura D, Yamada S, Sugahara K, Sasaki M, Kimura T (2011) Paradoxical effects of chondroitin sulfate-E on Japanese encephalitis viral infection. Biochem Biophys Res Commun 409:717–722Google Scholar
  82. Kim S-H, Turnbull J, Guimond SJ (2011) Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. Endocrinology 209:139–151Google Scholar
  83. Kirn-Safran CB, D’Souza SS, Carson DD (2008) Heparan sulfate proteoglycans and their binding proteins in embryo implantation and placentation. Semin Cell Dev Biol 19:187–193CrossRefGoogle Scholar
  84. Kobayashi F, Yamada S, Taguwa S, Kataoka C, Naito S, Hama Y, Tani H, Matsuura Y, Sugahara K (2012) Specific interaction of the envelope glycoproteins E1 and E2 with liver heparan sulfate involved in the tissue tropismatic infection by hepatitis C virus. Glycoconj J 29:211–220CrossRefGoogle Scholar
  85. Kozlowski EO, Pavao MSG (2011) Effect of sulfated glycosaminoglycans on tumor invasion and metastasis. Front Biosci Sch Ed S3:1541–1551CrossRefGoogle Scholar
  86. Kozlowski EO, Pavao MSG, Borsig L (2011) Ascidian dermatan sulfates attenuate metastasis, inflammation and thrombosis by inhibition of P-selectin. J Thromb Haemost 9:1807–1815CrossRefGoogle Scholar
  87. Krichen F, Volpi N, Sila A, Maccari F, Mantovani V, Galeotti F, Ellouz-Chaabouni S, Bougatef A (2017) Purification, structural characterization and antiproliferative properties of chondroitin sulfate/dermatan sulfate from tunisian fish skins. Int J Biol Macromol 95:32–39CrossRefGoogle Scholar
  88. Kroma A, Feliczak-Guzik A, Nowak I (2012) The use of glycosaminoglycans in cosmetic products. Chemik 66:136–139Google Scholar
  89. Kwok JCF, Warren P, Fawcett JW (2012) Chondroitin sulfate: a key molecule in the brain matrix. Int J Biochem Cell Biol 44:582–586CrossRefGoogle Scholar
  90. Ladet S (2013) Multilayer implants for delivery of therapeutic agents. PCT Int Appl WO 2013046057Google Scholar
  91. Lee EC, Davis-Poynter N, Nguyen CTH, Peters AA, Monteith GR, Strounina E, Popat A, Ross BP (2016) GAG mimetic functionalised solid and mesoporous silica nanoparticles as viral entry inhibitors of herpes simplex type 1 and type 2 viruses. Nanoscale 8:16192–16196CrossRefGoogle Scholar
  92. Lee-Sayer SSM, Dong Y, Arif AA, Olsson M, Brown KL, Johnson P (2015) The where, when, how, and why of hyaluronan binding by immune cells. Front Immunol 6:150CrossRefGoogle Scholar
  93. Ley K, Cerrito M, Arfors KE (1991) Sulfated polysaccharides inhibit leukocyte rolling in rabbit mesentery venules. Am J Phys 260:1667–1673Google Scholar
  94. Li Y, Liu Y, Xia W, Lei D, Voorhees JJ, Fisher GJ (2013) Age-dependent alterations of decorin glycosaminoglycans in human skin. Sci Rep 3:2422. 8 ppCrossRefGoogle Scholar
  95. Lian W, Wu M, Huang N, Gao N, Xiao C, Li Z, Zhang Z, Zheng Y, Peng W, Zhao J (2013) Anti-HIV-1 activity and structure-activity-relationship study of a fucosylated glycosaminoglycan from an echinoderm by targeting the conserved CD4 induced epitope. Biochim Biophys Acta 1830:4681–4691CrossRefGoogle Scholar
  96. Liang Y, Kiick KL (2014) Heparin-functionalized polymeric biomaterials in tissue engineering and drug delivery applications. Acta Biomater 10:1588–1600CrossRefGoogle Scholar
  97. Liaw PC, Becker DL, Stafford AR, Fredenburgh JC, Weitz JI (2001) Molecular basis for the susceptibility of fibrin-bound thrombin to inactivation by heparin cofactor II in the presence of dermatan sulfate but not heparin. J Biol Chem 276:20959–20965CrossRefGoogle Scholar
  98. Lin H-Y (2015) Compound of glycosaminoglycan, preparation method and use thereof. PCT Int Appl WO 2015/028172 A1; US Patent Appl Publ US 20150065446Google Scholar
  99. Liu L, Liu Y, Li J, Du G, Chen J (2011) Microbial production of hyaluronic acid: current state, challenges, and perspectives. Microb Cell Factories 10:99–108CrossRefGoogle Scholar
  100. Liu C-C, Zhao N, Kanekiyo T, Yamaguchi Y, Cirrito JR, Holtzman DM, Bu G (2016) Neuronal heparan sulfates promote amyloid pathology by modulating brain amyloid-β clearance and aggregation in Alzheimer’s disease. Sci Transl Med 8:332ra44CrossRefGoogle Scholar
  101. Lompardía SL, Díaz M, Papademetrio DL, Mascaró M, Pibuel M, Álvarez E, Hajos SE (2016) Hyaluronan oligomers sensitize chronic myeloid leukemia cell lines to the effect of Imatinib. Glycobiology 26:343–352CrossRefGoogle Scholar
  102. Lundin A, Bergström T, Andrighetti-Fröhner CR, Bendrioua L, Ferro V, Trybala E (2012) Potent anti-respiratory syncytial virus activity of a cholestanol-sulfated tetrasaccharide conjugate. Antivir Res 93:101–109CrossRefGoogle Scholar
  103. Manveen K, Sethi MK, Zaia J (2017) Extracellular matrix proteomics in schizophrenia and Alzheimer’s disease. Anal Bioanal Chem 409:379–394CrossRefGoogle Scholar
  104. Marchi E, Tamagnone G (1994) Method of treatment of diabetic nephropathy by means of sulodexide of medicines containing it. US Patent 5,496,807Google Scholar
  105. Martín R, Martín C, Escobedo S, Suárez JE, Quirós LM (2013) Surface glycosaminoglycans mediate adherence between HeLa cells and lactobacillus salivarius Lv72. BMC Microbiol 13:210. 11 ppCrossRefGoogle Scholar
  106. Martinez P, Vergoten G, Colomb F, Bobowski M, Steenackers A, Carpentier M, Allain F, Delannoy P, Julien S (2013) Over-sulfated glycosaminoglycans are alternative selectin ligands: insights into molecular interactions and possible role in breast cancer metastasis. Clin Exp Metastasis 30:919–931CrossRefGoogle Scholar
  107. Matheny RG (2015) Compositions and methods for preventing cardiac arrhythmia. US Patent 2015/0164959 A1Google Scholar
  108. Mathieu C, Dhondt KP, Chalons M, Mely S, Raoul H, Negre D, Cosset F-L, Gerlier D, Vives RR, Horvat B (2015) Heparan sulfate-dependent enhancement of henipavirus infection. MBio 6:1–10CrossRefGoogle Scholar
  109. Memi E, Karakiulakis G, Goma F, Papakonstantinou E (2012) The functional role of glycosaminoglycans in the pathophysiology of the thyroid gland and their putative role as prognostic, diagnostic and therapeutic agents in thyroid pathologies. Rev Clin Pharmacol Pharmacokinet Int Ed 26:61–86Google Scholar
  110. Mikami T, Kitagawa H (2013) Biosynthesis and function of chondroitin sulfate. Biochim Biophys Acta Gen Subj 1830:4719–4733CrossRefGoogle Scholar
  111. Misra S, Hascall VC, Markwald RR, Ghatak S (2015) Interactions between hyaluronan and its receptors (CD44, RHAMM) regulate the activities of inflammation and cancer. Front Immunol 6:201. 31 ppCrossRefGoogle Scholar
  112. Mizumoto S, Sugahara (2013) Glycosaminoglycans are functional ligands for receptor for advanced glycation end-products in tumors. FEBS J 280:2462–2470CrossRefGoogle Scholar
  113. Mizumoto S, Takahashi J, Sugahara K (2012) Receptor for advanced glycation end products (RAGE) functions as receptor for specific sulfated glycosaminoglycans, and anti-RAGE antibody or sulfated glycosaminoglycans delivered in vivo inhibit pulmonary metastasis of tumor cells. J Biol Chem 287:18985–18994CrossRefGoogle Scholar
  114. Monfort J, Pelletier J-P, Garcia-Giralt N, Martel-Pelletier J (2008) Biochemical basis of the effect of chondroitin sulphate on osteoarthritis articular tissues. Ann Rheum Dis 67:735–740CrossRefGoogle Scholar
  115. Mousa SA (2015) Composition and method for sulfated non-anticoagulant low molecular weight heparins in cancer and tumor metastasis. US Patent Appl Publ US 20150132399Google Scholar
  116. Mousa SA (2016) Composition and method of use for combinations of anti-viral protease, polymerase inhibitors and natural bioactive compounds in the treatment of hepatitis C infection. US Patent Appl Publ US20160346308 A1Google Scholar
  117. Murphy CM, Duffy GP, Schindeler A, O’Brien FJ (2016) Effect of collagen-glycosaminoglycan scaffold pore size on matrix mineralization and cellular behavior in different cell types. J Biomed Mater Res Part A 104:291–304CrossRefGoogle Scholar
  118. Nakano T, Betti M, Pietrasik Z (2010) Extraction, isolation and analysis of chondroitin sulfate glycosaminoglycans. Recent Pat Food Nutr Agric 2:61–74CrossRefGoogle Scholar
  119. Nickel JC, Egerdie RB, Steinhoff G, Palmer B, Hanno P (2010) A multicenter, randomized, double-blind, parallel group pilot evaluation of the efficacy and safety of intravesical sodium chondroitin sulfate versus vehicle control in patients with interstitial cystitis/painful bladder syndrome. Urology 76:804–809CrossRefGoogle Scholar
  120. Nikitovic D, Chatzinikolaou G, Tsiaoussis J, Tsatsakis A, Karamanos NK, Tzanakakis GN (2012) Insights into targeting colon cancer cell fate at the level of proteoglycans/glycosaminoglycans. Curr Med Chem 19:4247–4258CrossRefGoogle Scholar
  121. Nishimura Y, Shudo H, Seto H, Hoshino Y, Miura Y (2013) Syntheses of sulfated glycopolymers and analyses of their BACE-1 inhibitory activity. Bioorg Med Chem Lett 23:6390–6395CrossRefGoogle Scholar
  122. Nugent MA (2000) Heparin sequencing brings structure to the function of complex oligosaccharides. Proc Natl Acad Sci U S A 97:10301–10303CrossRefGoogle Scholar
  123. O'Hearn A, Wang M, Cheng H, Lear-Rooney CM, Koning K, Rumschlag-Booms E, Varhegyi E, Olinger G, Rong L (2015) Role of EXT1 and glycosaminoglycans in the early stage of filovirus entry. J Virol 89:5441–5449CrossRefGoogle Scholar
  124. Papakonstantinou E, Roth M, Karakiulakis G (2012) Hyaluronic acid: a key molecule in skin aging. Dermato-Endocrinol 4:253–258CrossRefGoogle Scholar
  125. Papy-Garcia D, Christophe M, Huynh MB, Sineriz F, Sissoeff L, Sepulveda-Diaz JE, Raisman-Vozari R (2011) Glycosaminoglycans, protein aggregation and neurodegeneration. Curr Protein Pept Sci 12:258–268CrossRefGoogle Scholar
  126. Papy-Garcia D, Huynh MB, Soussi-Yanicostas N, Vozari R, Sineriz F, Yanicostas C (2013) Method of diagnosis, prognosis, or treatment of neurodegenerative diseases. PCT Int Appl WO 2013/053954.Google Scholar
  127. Paul TJ, Kelly H, Zuchniarz J, Ahmed T, Prabhakar R (2016) Design of heparin oligosaccharide based molecules for inhibition of Alzheimer amyloid beta (Aβ40) aggregation. Can J Chem 94:1090–1098CrossRefGoogle Scholar
  128. Peer D (2015) Liposomal formulations for delivery of nucleic acids. Int Appl WO 2015/198326Google Scholar
  129. Persson A, Tykesson E, Westergren-Thorsson G, Malmström A, Ellervik U, Mani K (2016) Xyloside-primed chondroitin sulfate/dermatan sulfate from breast carcinoma cells with a defined disaccharide composition has cytotoxic effects in vitro. J Biol Chem 291:14871–14882CrossRefGoogle Scholar
  130. Petrey AC, de la Motte CA (2014) Hyaluronan, a crucial regulator of inflammation. Front Immunol 5:101CrossRefGoogle Scholar
  131. Pisano C, Vlodavsky I, Ilan N, Zunino F (2014) The potential of heparanase as a therapeutic target in cancer. Biochem Pharmacol 89:12–19CrossRefGoogle Scholar
  132. Pomin VH (2015a) A dilemma in the glycosaminoglycan-based therapy: synthetic or naturally unique molecules? Med Res Rev 35:1195–1219CrossRefGoogle Scholar
  133. Pomin VH (2015b) Sulfated glycans in inflammation. Eur J Med Chem 92:353–369CrossRefGoogle Scholar
  134. Pomin VH, Mulloy B (2015) Current structural biology of the heparin interactome. Curr Opin Struct Biol 34:17–25CrossRefGoogle Scholar
  135. Prestwich GD, Kennedy TP (2011) Methods for treating or preventing the spread of cancer using semi-synthetic glycosaminoglycosan ethers. PCT Int Appl WO 2011/094149Google Scholar
  136. Prestwich GD, Oottamasathein S, Kennedy T (2011) Applications of partially and fully sulfated hyaluronan. PCT Int Appl WO 2011/156445Google Scholar
  137. Prestwich GD, Oottamasathien S, Kennedy TP (2013) Applications of partially and fully sulfated hyaluronan. US Patent Appl 0,209,531Google Scholar
  138. Puperi DS, O’Connell RW, Punske ZE, Wu Y, West JL, Grande-Allen KJ (2016) Hyaluronan hydrogels for a biomimetic spongiosa layer of tissue engineered heart valve scaffolds. Biomacromolecules 17:1766–1775CrossRefGoogle Scholar
  139. Pye DA, Ogundipe OD (2016) Pharmaceutical extracts and uses thereof. PCT Int Appl WO 2016/067008Google Scholar
  140. Qian W, Tao L, Wang Y, Zhang F, Li M, Huang S, Wang A, Chen W, Yue Z, Chen L, Liu Y, Huang C, Zhang L, Li Y, Lu Y (2015) Downregulation of integrins in cancer cells and anti-platelet properties are involved in holothurian glycosaminoglycan-mediated disruption of the interaction of cancer cells and platelets in hematogenous metastasis. J Vasc Res 52:197–209CrossRefGoogle Scholar
  141. Radhakrishnan K, Tripathy J, Datey A, Chakravortty D, Raichur AM (2015) Mesoporous silica-chondroitin sulphate hybrid nanoparticles for targeted and bio-responsive drug delivery. New J Chem 39:1754–1760CrossRefGoogle Scholar
  142. Rankin KS, Frankel D (2016) Hyaluronan in cancer – from the naked mole rat to nanoparticle therapy. Soft Matter 12:3841–3848CrossRefGoogle Scholar
  143. Rawat M, Hsieh-Wilson L (2014) Glycosaminoglycan mimetics. US Patent 8,912,149 B1Google Scholar
  144. Reinmueller J, Dirting K (2012) Antiinfective composition. PCT Int Appl WO 2012/168462; Ger Offen DE 102011077393Google Scholar
  145. Ren X, Weisgerber DW, Bischoff D, Lewis MS, Reid RR, He T-C, Yamaguchi DT, Miller TA, Harley BAC, Lee JC (2016) Nanoparticulate mineralized collagen scaffolds and BMP-9 induce a long-term bone cartilage construct in human mesenchymal stem cells. Adv Healthc Mater 5:1821–1830CrossRefGoogle Scholar
  146. Rilla K, Tiihonen R, Kultti A, Tammi M, Tammi R (2008) Pericellular hyaluronan coat visualized in live cells with a fluorescent probe is scaffolded by plasma membrane protrusions. J Histochem Cytochem 56:901–910CrossRefGoogle Scholar
  147. Ritchie JP, Ramani VC, Ren Y, Naggi A, Torri G, Casu B, Penco S, Pisano C, Carminati P, Tortoreto M, Zunino F, Vlodavsky I, Sanderson RD, Yang Y (2011) SST0001, a chemically modified heparin, inhibits myeloma growth and angiogenesis via disruption of the heparanase/syndecan-1 axis. Clin Cancer Res 17:1382–1393CrossRefGoogle Scholar
  148. Ronca F, Palmieri L, Panicucci P, Ronca G (1998) Anti-inflammatory activity of chondroitin sulfate. Osteoarthr Cartil 6(Suppl A):14–21CrossRefGoogle Scholar
  149. Said JS, Trybala E, Görander S, Ekblad M, Liljeqvist J-A, Jennische E, Lange S, Bergström T (2016) The cholestanol-conjugated sulfated oligosaccharide PG545 disrupts the lipid envelope of herpes simplex virus particles. Antimicrob Agents Chemother 60:1049–1057CrossRefGoogle Scholar
  150. Sakiyama-Elbert SE (2014) Incorporation of heparin into biomaterials. Acta Biomater 10:1581–1587CrossRefGoogle Scholar
  151. Salbach J, Rachner TD, Rauner M, Hempel U, Anderegg U, Franz S, Simon J-C, Hofbauer LC (2012) Regenerative potential of glycosaminoglycans for skin and bone. J Mol Med 90:625–635CrossRefGoogle Scholar
  152. Savage JR, Pulsipher A, Rao NV, Kennedy TP, Prestwich GD, Ryan ME, Lee WY (2016) A modified glycosaminoglycan, GM-0111, inhibits molecular signaling involved in periodontitis. PLoS One 11:e0157310/1Google Scholar
  153. Sayari N, Balti R, Ben Mansour M, Ben Amor I, Graiet I, Gargouri J, Bougatef A (2016) Anticoagulant properties and cytotoxic effect against HCT116 human colon cell line of sulfated glycosaminoglycans isolated from the Norway lobster (Nephrops norvegicus) shell. Biomed Pharmacother 80:322–330CrossRefGoogle Scholar
  154. Schaefer L, Schaefer RM (2010) Proteoglycans: from structural compounds to signaling molecules. Cell Tissue Res 339:237–246CrossRefGoogle Scholar
  155. Schnabelrauch M, Scharnweber D, Schiller J (2013) Sulfated glycosaminoglycans as promising artificial extracellular matrix components to improve the regeneration of tissues. J Curr Med Chem 20:2501–2523CrossRefGoogle Scholar
  156. Schwoerer R, Zubkova OV, Turnbull JE, Tyler PC (2013) Synthesis of a targeted library of heparan sulfate hexa- to dodecasaccharides as inhibitors of β-secretase: potential therapeutics for Alzheimer’s disease. Chem Eur J 19:6817–6823Google Scholar
  157. Scott IR (1988) Skin treatment composition. EP 0295092 B1Google Scholar
  158. Seki Y, Mizukura M, Ichimiya T, Suda Y, Nishihara S, Masuda M, Takase-Yoden S (2012) O-sulfate groups of heparin are critical for inhibition of ecotropic murine leukemia virus infection by heparin. Virology 424:56–66CrossRefGoogle Scholar
  159. Silva LA, Khomandiak S, Ashbrook AW, Weller R, Heise MT, Morrison TE, Dermody TS (2014) A single-amino-acid polymorphism in chikungunya virus E2 glycoprotein influences glycosaminoglycan utilization. J Virol 88:2385–2397CrossRefGoogle Scholar
  160. Simionescu D, Mercuri JJ (2016). Shape-memory sponge hydrogel biomaterial. US Patent 9,283,301Google Scholar
  161. Spero M, Weiss MS, Kopp JB (2005) Methods using glycosaminoglycans for the treatment of kidney disease. PCT Int Appl WO 2006039709 A1Google Scholar
  162. Staples GO, Zaia J (2011) Mass spectrometry in carbohydrate sequencing and binding analysis. In: Wang B, Boons G-J (eds) Carbohydrate recognition: biological problems, methods, and applications. Wiley, Hoboken, pp 257–300CrossRefGoogle Scholar
  163. Stern R, Maibach HI (2008) Hyaluronan in skin: aspects of aging and its pharmacologic modulation. Clin Dermatol 26:106–122CrossRefGoogle Scholar
  164. Stewart KL, Hughes E, Yates EA, Akien GR, Huang T-Y, Lima MA, Rudd TR, Guerrini M, Hung S-C, Radford SE, Middleton DA (2016) Atomic details of the interactions of glycosaminoglycans with amyloid β fibrils. J Am Chem Soc 138:8328–8331CrossRefGoogle Scholar
  165. Ströh LJ, Stehle T (2014) Glycan engagement by viruses: receptor switches and specificity. Ann Rev Virol 1:285–306CrossRefGoogle Scholar
  166. Tangso KJ, da Cunha PHCD, Spicer P, Li J, Boyd BJ (2016) Antimicrobial activity from colistin-heparin lamellar-phase complexes for the coating of biomedical devices. ACS Appl Mater Interfaces 8:31321–31329CrossRefGoogle Scholar
  167. Theocharis AD, Skandalis SS, Gialeli C, Karamanos NK (2016) Extracellular matrix structure. Adv Drug Deliv Rev 97:4–27CrossRefGoogle Scholar
  168. Turley E (2010) Topically administered, skin-penetrating glycosaminoglycan formulations suitable for use in cosmetic and pharmaceutical applications. CA 2703532 A1; PCT Int Appl WO 2011/140630 A1Google Scholar
  169. Tyler PC, Guimond SE, Turnbull JE, Zubkova OV (2015) Single-entity heparan sulfate glycomimetic clusters for therapeutic applications. Angew Chem Int Ed 54:2718–2723CrossRefGoogle Scholar
  170. Verges Milano J, Garcia Garcia A, Ruhi Roura R, Montell Bonaventura E, Garcia Lopez M, Alaez Verson CR, Escaich Ferrer J, Egea Maiquez J, Lorrio Gonzalez S, Negredo Madrigal P (2011) Sulphated disaccharides for the treatment of neurodegenerative and/or neurovascular diseases. PCT Int. Appl. WO 2011/080203Google Scholar
  171. Vistoli G, De Maddis D, Cipak A, Zarkovic N, Carini M, Aldini G (2013) Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radic Res 47:3–27CrossRefGoogle Scholar
  172. Volpi N, Schiller J, Stern R, Soltes L (2009) Role, metabolism, chemical modifications and applications of hyaluronan. Curr Med Chem 16:1718–1745CrossRefGoogle Scholar
  173. Von Recum HA, Hijaz A (2014) Glycosaminoglycans for chemokine drug delivery. U.S. Pat. Appl. Publ. US 20140364360Google Scholar
  174. Vuillermoz B, Wegrowski Y, Contet-Audonneau J-L, Danoux L, Pauly G, Maquart F-X (2005) Influence of aging on glycosaminoglycans and small leucine-rich proteoglycans production by skin fibroblasts. Mol Cell Biochem 277:63–72CrossRefGoogle Scholar
  175. Wang P, Ding K (2014) Proteoglycans and glycosaminoglycans in misfolded proteins formation in Alzheimer’s disease. Protein Pept Lett 21:1048–1056CrossRefGoogle Scholar
  176. Weigel PH, Fuller GM, LeBoeuf RD (1986) A model for the role of hyaluronic acid and fibrin in the early events during the inflammatory response and wound healing. J Theor Biol 119:219–234CrossRefGoogle Scholar
  177. Wu RL, Huang L, Zhao H-C, Geng X-P (2017) Hyaluronic acid in digestive cancers. J Cancer Res Clin Oncol 143:1–16CrossRefGoogle Scholar
  178. Xiao L, Tong Z, Chen Y, Pochan DJ, Sabanayagam CR, Jia X (2013) Hyaluronic acid-based hydrogels containing covalently integrated drug depots: implication for controlling inflammation in mechanically stressed tissues. Biomacromolecules 14:3808–3819CrossRefGoogle Scholar
  179. Xu D, Olson J, Cole JN, van Wijk XM, Brinkmann V, Zychlinsky A, Nizet V, Esko JD, Chang Y-C (2015) Heparan sulfate modulates neutrophil and endothelial function in antibacterial innate immunity. Infect Immun 83:3648–3656CrossRefGoogle Scholar
  180. Yang R-M, Fu C-P, Li N-N, Wang L, Xu X-D, Yang D-Y, Fang J-Z, Jiang X-Q, Zhang L-M (2014) Glycosaminoglycan-targeted iron oxide nanoparticles for magnetic resonance imaging of liver carcinoma. Mater Sci Eng C Mater Biol Appl 45:556–563CrossRefGoogle Scholar
  181. Yang X, Du H, Liu J, Zhai G (2015) Advanced nanocarriers based on heparin and its derivatives for cancer management. Biomacromolecules 16:423–436CrossRefGoogle Scholar
  182. Yip GW, Smollich M, Götte M (2006) Therapeutic value of glycosaminoglycans in cancer. Mol Cancer Ther 5:2139–2148CrossRefGoogle Scholar
  183. Yue Z, Wang A, Zhu Z, Tao L, Li Y, Zhou L, Chen W, Lu Y (2015) Holothurian glycosaminoglycan inhibits metastasis via inhibition of P-selectin in B16F10 melanoma cells. Mol Cell Biochem 410:143–154CrossRefGoogle Scholar
  184. Yuk SH, Oh KS, Cho SH, Lee BS, Kim SY, Kwak BK, Kim K, Kwon IC (2011) Glycol chitosan/heparin immobilized iron oxide nanoparticles with a tumor-targeting characteristic for magnetic resonance imaging. Biomacromolecules 12:2335–2343CrossRefGoogle Scholar
  185. Zhang Q, Li J, Liu C, Song C, Li P, Yin F, Xiao Y, Jiang W, Zong A, Zhang X, Wang F (2015) Protective effects of low molecular weight chondroitin sulfate on amyloid beta (Aβ)-induced damage in vitro and in vivo. Neuroscience 305:169–182CrossRefGoogle Scholar
  186. Zhang RR, Strebe JK, Kuo JS (2016) Heparan sulfates promote amyloid pathology in Alzheimer disease. Neurosurgery 79:N12–N13Google Scholar
  187. Zhang X, Zhao X, Lang Y, Li Q, Liu X, Cai C, Hao J, Li G, Yu G (2016) Low anticoagulant heparin oligosaccharides as inhibitors of BACE-1, the Alzheimer’s β-secretase. Carbohydr Polym 151:51–59Google Scholar
  188. Zhao W, McCallum SA, Xiao Z, Zhang F, Linhardt RJ (2012) Binding affinities of vascular endothelial growth factor (VEGF) for heparin-derived oligosaccharides. Biosci Rep 32:71–81CrossRefGoogle Scholar
  189. Zheng S, Jin Z, Han J, Cho S, Nguyen VD, Young Ko S, Park J-O, Park S (2016) Preparation of HIFU-triggered tumor-targeted hyaluronic acid micelles for controlled drug release and enhanced cellular uptake. Colloids Surf B: Biointerfaces 143:27–36CrossRefGoogle Scholar
  190. Zhong WP, Chin HG, Lee EJ, Guo S, Yip GW, Lam Y (2015) Divergent synthesis of chondroitin sulfate disaccharides and identification of sulfate motifs that inhibit triple negative breast cancer. Sci Rep 5:14355. 8 ppCrossRefGoogle Scholar
  191. Zhou X, Jin L (2016) The structure-activity relationship of glycosaminoglycans and their analogues with β-amyloid peptide. Protein Pept Lett 23:358–364CrossRefGoogle Scholar
  192. Zhou H, Roy S, Cochran E, Zouaoui R, Chu CL, Duffner J, Zhao G, Smith S, Galcheva-Gargova Z, Karlgren J, Dussault N, Kwan RY, Moy E, Barnes M, Long A, Honan C, Qi YW, Shriver Z, Ganguly T, Schultes B, Venkataraman G, Kishimoto TK (2011) M402, a novel heparan sulfate mimetic, targets multiple pathways implicated in tumor progression and metastasis. PLoS One 6:e21106CrossRefGoogle Scholar
  193. Zhu M, Feng Q, Sun Y, Li G, Bian L (2016) Effect of cartilaginous matrix components on the chondrogenesis and hypertrophy of mesenchymal stem cells in hyaluronic acid hydrogels. J Biomed Mater Res Part B Appl Biomater. doi: 10.1002/jbm.b.33760
  194. Zieris A, Dockhorn R, Röhrich A, Zimmermann R, Müller M, Welzel PB, Tsurkan MV, Sommer J-U, Freudenberg U, Werner C (2014) Biohybrid networks of selectively desulfated glycosaminoglycans for tunable growth factor delivery. Biomacromolecules 55:4439–4446CrossRefGoogle Scholar
  195. Zimmer R, Courty J (2012) Compositions comprising multivalent synthetic ligands of surface nucleolin and glycosaminoglycans. PCT Int Appl WO 2012/045750Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • José Kovensky
    • 1
  • Eric Grand
    • 1
  • María Laura Uhrig
    • 2
    • 3
  1. 1.Laboratoire de Glycochimie, des Antimicrobiens et des Agroressources (LG2A) CNRS UMR 7378, Institut de Chimie de Picardie CNRS FR 3085Université de Picardie Jules VerneAmiens CedexFrance
  2. 2.Facultad de Ciencias Exactas y Naturales, Departamento de Química OrgánicaUniversidad de Buenos Aires, Pabellón 2, Ciudad UniversitariaBuenos AiresArgentina
  3. 3.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)-UBA, Centro de Investigación en Hidratos de Carbono (CIHIDECAR)Buenos AiresArgentina

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