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Uronic Acids in Oligosaccharide and Glycoconjugate Synthesis

  • Jeroen D. C. Codée
  • Alphert E. Christina
  • Marthe T. C. Walvoort
  • Herman S. Overkleeft
  • Gijsbert A. van der Marel
Part of the Topics in Current Chemistry book series (TOPCURRCHEM, volume 301)

Abstract

This chapter describes the assembly of uronic acid containing oligosaccharides and glycoconjugates. Two strategies are available to access these target molecules, namely a pre-glycosylation oxidation approach, in which uronic acid building blocks are used, and a post-glycosylation oxidation strategy, which employs an oxidation step after the assembly of the oligosaccharide chain. Because uronic acid building blocks are generally considered to be less reactive than their non-oxidized counterparts, the latter approach has found most application in carbohydrate synthesis. With the aid of selected examples of recent syntheses of biologically relevant oligosaccharides and glycoconjugates, the reactivity of different uronic acid building blocks is evaluated. From these examples it is apparent that the generally assumed low reactivity of uronic acids does not a priori rule out an efficient assembly of these target compounds. Besides influencing the reactivity of a given pyranoside, the C-5 carboxylic acid function can also have a profound effect on the stereochemical course of a glycosylation reaction, which can be exploited in the stereoselective formation of glycosidic bonds.

Keywords

Glycosylation Reactivity Stereoselectivity Uronic acids 

References

  1. 1.
    Lindberg B, Kenne L (1985) The polysaccharides. Academic, New YorkGoogle Scholar
  2. 2.
    Van den Bos LJ, Codée JDC, Litjens REJN, Dinkelaar J, Overkleeft HS, Van der Marel GA (2007) Uronic acids in oligosaccharide synthesis. Eur J Org Chem 3963–3976Google Scholar
  3. 3.
    Hassan H (2007) Present status in the chemistry of hexuronic acids found in glycosaminoglycans and their mimetic aza-sugars analogues. Mini-Rev Org Chem 4:61–74Google Scholar
  4. 4.
    Schmidt RR, Grundler G (1981) Simple synthesis of β-D-glucopyranosyluronates. Synthesis 885–887Google Scholar
  5. 5.
    Schmidt RR, Stumpp M, Michel J (1982) Glycosylimidates 4. α-D-Glucopyranosyl and β-D-glucopyranosyl phosphates from O-α-D-glucopyranosyl trichloroacetimidates. Tetrahedron Lett 23:405–408Google Scholar
  6. 6.
    Veeneman GH, Van Leeuwen SH, Van Boom JH (1990) Iodonium ion promoted reactions at the anomeric center 2. An efficient thioglycoside mediated approach toward the formation of 1, 2-trans linked glycosides and glycosidic esters. Tetrahedron Lett 31:1331–1334Google Scholar
  7. 7.
    Fraser-Reid B, Wu ZF, Udodong UE, Ottosson H (1990) Armed-disarmed effects in glycosyl donors – rationalization and sidetracking. J Org Chem 55:6068–6070Google Scholar
  8. 8.
    Veeneman GH, van Boom JH (1990) An efficient thioglycoside-mediated formation of α-glycosidic linkages promoted by iodonium dicollidine perchlorate. Tetrahedron Lett 31:275–278Google Scholar
  9. 9.
    Douglas NL, Ley SV, Lucking U, Warriner SL (1998) Tuning glycoside reactivity: new tool for efficient oligosaccharide synthesis. J Chem Soc Perkin Trans 1:51–65Google Scholar
  10. 10.
    Zhang ZY, Ollmann IR, Ye XS, Wischnat R, Baasov T, Wong CH (1999) Programmable one-pot oligosaccharide synthesis. J Am Chem Soc 121:734–753Google Scholar
  11. 11.
    Koeller KM, Wong CH (2000) Synthesis of complex carbohydrates and glycoconjugates: enzyme-based and programmable one-pot strategies. Chem Rev 100:4465–4493Google Scholar
  12. 12.
    Jensen HH, Lyngbye L, Jensen A, Bols M (2002) Stereoelectronic substituent effects in polyhydroxylated piperidines and hexahydropyridazines. Chem Eur J 8:1218–1226Google Scholar
  13. 13.
    Shipkova M, Wieland E (2005) Glucuronidation in therapeutic drug monitoring. Clin Chim Acta 358:2–23Google Scholar
  14. 14.
    Shipkova M, Armstrong VW, Oellerich M, Wieland E (2003) Acyl glucuronide drug metabolites: toxicological and analytical implications. Ther Drug Monit 25:1–16Google Scholar
  15. 15.
    Stachulski AV, Harding JR, Lindon JC, Maggs JL, Park BK, Wilson ID (2006) Acyl glucuronides: biological activity, chemical reactivity, and chemical synthesis. J Med Chem 49:6931–6945Google Scholar
  16. 16.
    Stachulski AV, Jenkins GN (1998) The synthesis of O-glucuronides. Nat Prod Rep 15:173–186Google Scholar
  17. 17.
    Kaspersen FM, Van Boeckel CAA (1987) A review of the methods of chemical synthesis of sulfate and glucuronide conjugates. Xenobiotica 17:1451–1471Google Scholar
  18. 18.
    Lucas R, Alcantara D, Morales JC (2009) A concise synthesis of glucuronide metabolites of urolithin-B, resveratrol, and hydroxytyrosol. Carbohydr Res 344:1340–1346Google Scholar
  19. 19.
    Juteau H, Gareau Y, Labelle M (1997) A convenient synthesis of β-acyl glucuronides. Tetrahedron Lett 38:1481–1484Google Scholar
  20. 20.
    Perrie JA, Harding JR, Holt DW, Johnston A, Meath P, Stachulski AV (2005) Effective synthesis of 1-β-acyl glucuronides by selective acylation. Org Lett 7:2591–2594Google Scholar
  21. 21.
    Jones AE, Wilson HK, Meath P, Meng XL, Holt DW, Johnston A, Oellerich M, Armstrong VW, Stachulski AV (2009) Convenient syntheses of the in vivo carbohydrate metabolites of mycophenolic acid: reactivity of the acyl glucuronide. Tetrahedron Lett 50:4973–4977Google Scholar
  22. 22.
    Bowkett ER, Harding JR, Maggs JL, Park BK, Perrie JA, Stachulski AV (2007) Efficient synthesis of 1-β-O-acyl glucuronides via selective acylation of allyl or benzyl D-glucuronate. Tetrahedron 63:7596–7605Google Scholar
  23. 23.
    Vincken J-P, Heng L, Groot AD, Gruppen H (2007) Saponins, classification and occurrence in the plant kingdom. Phytochemistry 68:275–297Google Scholar
  24. 24.
    Hostettmann K, Marston A (1995) Saponins. Cambridge University Press, CambridgeGoogle Scholar
  25. 25.
    Yu BA, Sun JS (2009) Current synthesis of triterpene saponins. Chem Asian J 4:642–654Google Scholar
  26. 26.
    Yu B, Zhang YC, Tang PP (2007) Carbohydrate chemistry in the total synthesis of Saponins. Eur J Org Chem 5145–5161Google Scholar
  27. 27.
    Kensil CR (1996) Saponins as vaccine adjuvants. Crit Rev Ther Drug Carrier Syst 13:1–55Google Scholar
  28. 28.
    Cleland JL, Kensil CR, Lim A, Jacobsen NE, Basa L, Spellman M, Wheeler DA, Wu JY, Powell MF (1996) Isomerization and formulation stability of the vaccine adjuvant QS-21. J Pharm Sci 85:22–28Google Scholar
  29. 29.
    Jacobsen NE, Fairbrother WJ, Kensil CR, Lim A, Wheeler DA, Powell MF (1996) Structure of the saponin adjuvant QS-21 and its base-catalyzed isomerization product by H-1 and natural abundance C-13 NMR spectroscopy. Carbohydr Res 280:1–14Google Scholar
  30. 30.
    Kim YJ, Wang PF, Navarro-Villalobos M, Rohde BD, Derryberry J, Gin DY (2006) Synthetic studies of complex immunostimulants from Quillaja saponaria: synthesis of the potent clinical immunoadjuvant QS-21A(api). J Am Chem Soc 128:11906–11915Google Scholar
  31. 31.
    Kim YJ, Gin DY (2001) Synthesis of the trisaccharide portion of the immunologic adjuvant QS-21A via sulfonium-mediated oxidative and dehydrative glycosylation. Org Lett 3:1801–1804Google Scholar
  32. 32.
    Deng K, Adams MM, Damani P, Livingston PO, Ragupathi G, Gin DY (2008) Synthesis of QS-21-xylose: establishment of the immunopotentiating activity of synthetic QS-21 adjuvant with a melanoma vaccine. Angew Chem Int Ed 47:6395–6398Google Scholar
  33. 33.
    Adams MM, Damani P, Perl NR, Won A, Hong F, Livingston PO, Ragupathi G, Gin DY (2010) Design and synthesis of potent quillaja saponin vaccine adjuvants. J Am Chem Soc 132:1939–1945Google Scholar
  34. 34.
    Ishihara K, Yamamoto H (1999) Arylboron compounds as acid catalysts in organic synthetic transformations. Eur J Org Chem 527–538Google Scholar
  35. 35.
    Gallagher JT, Turnbull JE (1992) Heparan-sulfate in the binding and activation of fibroblast growth-factor. Glycobiol 2:523–528Google Scholar
  36. 36.
    Spillmann D, Lindahl U (1994) Glycosaminoglycan protein interactions: a question of specificity. Curr Opin Struct Biol 4:677–682Google Scholar
  37. 37.
    Capila I, Linhardt RJ (2002) Heparin-protein interactions. Angew Chem Int Ed 41:391–412Google Scholar
  38. 38.
    Noti C, Seeberger PH (2005) Chemical approaches to define the structure-activity relationship of heparin-like glycosaminoglycans. Chem Biol 12:731–756Google Scholar
  39. 39.
    Codée JDC, Overkleeft HS, van der Marel GA, van Boeckel CAA (2004) The synthesis of well-defined heparin and heparan sulfate fragments. Drug Discov Today Technol 1:317–326Google Scholar
  40. 40.
    Karst NA, Linhardt RJ (2003) Recent chemical and enzymatic approaches to the synthesis of glycosaminoglycan oligosaccharides. Curr Med Chem 10:1993–2031Google Scholar
  41. 41.
    Yeung BKS, Chong PYC, Petillo PA (2002) Synthesis of glycosaminoglycans. J Carbohydr Chem 21:799–865Google Scholar
  42. 42.
    Spijker NM, Van Boeckel CAA (1991) Double stereodifferentiation in carbohydrate coupling reactions – the mismatched interaction of donor and acceptor as an unprecedented factor in governing the α/β ratio of glycoside formation. Angew Chem Int Ed Engl 30:180–183Google Scholar
  43. 43.
    Spijker NM, Basten JEM, Van Boeckel CAA (1993) Unexpected phenomena in glycosylations of acceptors with L-idose configuration. Rec Trav Chim Pays-Bas 112:611–617Google Scholar
  44. 44.
    Arungundram S, Al-Mafraji K, Asong J, Leach FE III, Amster IJ, Venot A, Turnbull JE, Boons G-J (2009) Modular synthesis of heparan sulfate oligosaccharides for structure-activity relationship studies. J Am Chem Soc 131:17394–17405Google Scholar
  45. 45.
    De Mico A, Margarita R, Parlanti L, Vescovi A, Piancatelli G (1997) A versatile and highly selective hypervalent iodine (III)/2,2,6,6-tetramethyl-1-piperidinyloxyl-mediated oxidation of alcohols to carbonyl compounds. J Org Chem 62:6974–6977Google Scholar
  46. 46.
    Van den Bos LJ, Codee JDC, Van der Toorn JC, Boltje TJ, Van Boom JH, Overkleeft HS, Van der Marel GA (2004) Thioglycuronides: synthesis and application in the assembly of acidic oligosaccharides. Org Lett 6:2165–2168Google Scholar
  47. 47.
    Codée JDC, Stubba B, Schiattarella M, Overkleeft HS, van Boeckel CAA, van Boom JH, van der Marel GA (2005) A modular strategy toward the synthesis of heparin-like oligosaccharides using monomeric building blocks in a sequential glycosylation strategy. J Am Chem Soc 127:3767–3773Google Scholar
  48. 48.
    Polat T, Wong CH (2007) Anomeric reactivity-based one-pot synthesis of heparin-like oligosaccharides. J Am Chem Soc 129:12795–12800Google Scholar
  49. 49.
    Tamura J, Tokuyoshi M (2004) Synthesis of chondroitin sulfate E hexasaccharide in the repeating region by an effective elongation strategy toward longer chondroitin oligosaccharide. Biosci Biotech Biochem 68:2436–2443Google Scholar
  50. 50.
    Tamura JI, Nakada Y, Taniguchi K, Yamane M (2008) Synthesis of chondroitin sulfate E octasaccharide in a repeating region involving an acetamide auxiliary. Carbohydr Res 343:39–47Google Scholar
  51. 51.
    Crich D, Dudkin V (2001) Why are the hydroxyl groups of partially protected N-acetylglucosamine derivatives such poor glycosyl acceptors, and what can be done about it? A comparative study of the reactivity of N-acetyl, N-phthalimido, and 2-azido-2-deoxyglucosamine derivatives in glycosylation. 2-Picolinyl ethers as reactivity-enhancing replacements for benzyl ethers. J Am Chem Soc 123:6819–6825Google Scholar
  52. 52.
    Lopin C, Jacquinet JC (2006) From polymer to size-defined oligomers: an expeditious route for the preparation of chondroitin oligosaccharides. Angew Chem Int Ed Engl 45:2574–2578Google Scholar
  53. 53.
    Vibert A, Lopin-Bon C, Jacquinet JC (2009) From polymer to size-defined oligomers: a step economy process for the efficient and stereocontrolled construction of chondroitin oligosaccharides and biotinylated conjugates thereof: part 1. Chem Eur J 15:9561–9578Google Scholar
  54. 54.
    Jacquinet JC, Lopin-Bon C, Vibert A (2009) From polymer to size-defined oligomers: a highly divergent and stereocontrolled construction of chondroitin sulfate A, C, D, E, K, L, and M oligomers from a single precursor: part 2. Chem Eur J 15:9579–9595Google Scholar
  55. 55.
    Levene PA (1941) On chondrosin. J Biol Chem 140:267–277Google Scholar
  56. 56.
    Davidson EA, Meyer K (1954) Structural studies on chondroitin sulfuric acid: the nature of chondrosin. J Am Chem Soc 76:5686–5689Google Scholar
  57. 57.
    Belot F, Jacquinet JC (2000) Unexpected stereochemical outcome of activated 4,6-O-benzylidene derivatives of the 2-deoxy-2-trichloroacetamido-D-galacto series in glycosylation reactions during the synthesis of a chondroitin 6-sulfate trisaccharide methyl glycoside. Carbohydr Res 325:93–106Google Scholar
  58. 58.
    Jeanloz RW, Flowers HM (1962) Isolation and synthesis of methyl ester-methyl α-glycoside of 3-β-D-glucuronosyl-N-acetyl-D-glucosamine (hyalobiuronic acid). J Am Chem Soc 84:3030Google Scholar
  59. 59.
    Blatter G, Jacquinet JC (1996) The use of 2-deoxy-2-trichloroacetamido-D-glucopyranose derivatives in syntheses of hyaluronic acid-related tetra-, hexa-, and octa-saccharides having a methyl β-D-glucopyranosiduronic acid at the reducing end. Carbohydr Res 288:109–125Google Scholar
  60. 60.
    Dinkelaar J, Gold H, Overkleeft HS, Codee JDC, van der Marel GA (2009) Synthesis of hyaluronic acid oligomers using chemoselective and one-pot strategies. J Org Chem 74:4208–4216Google Scholar
  61. 61.
    Dinkelaar J, Codee JDC, van den Bos LJ, Overkleeft HS, van der Marel GA (2007) Synthesis of hyaluronic acid oligomers using Ph2SO/Tf2O-mediated glycosylations. J Org Chem 72:5737–5742Google Scholar
  62. 62.
    Huang LJ, Huang XF (2007) Highly efficient syntheses of hyaluronic acid oligosaccharides. Chem Eur J 13:529–540Google Scholar
  63. 63.
    Lu X, Kamat MN, Huang L, Huang X (2009) Chemical synthesis of a hyaluronic acid decasaccharide. J Org Chem 74:7608–7617Google Scholar
  64. 64.
    Codée JDC, Litjens REJN, Van den Bos LJ, Overkleeft HS, Van der marel GA (2005) Thioglycosides in sequential glycosylation strategies. Chem Soc Rev 34:769–782Google Scholar
  65. 65.
    Wang Y, Ye XS, Zhang LH (2007) Oligosaccharide assembly by one-pot multi-step strategy. Org Biomol Chem 5:2189–2200Google Scholar
  66. 66.
    Huang LJ, Teumelsan N, Huang XF (2006) A facile method for oxidation of primary alcohols to carboxylic acids and its application in glycosaminoglycan syntheses. Chem Eur J 12:5246–5252Google Scholar
  67. 67.
    Zeng YL, Wang Z, Whitfield D, Huang XF (2008) Installation of electron-donating protective groups, a strategy for glycosylating unreactive thioglycosyl acceptors using the preactivation-based glycosylation method. J Org Chem 73:7952–7962Google Scholar
  68. 68.
    Leone S, Silipo A, Nazarenko EL, Lanzetta R, Parrilli M, Molinaro A (2007) Molecular structure of endotoxins from Gram-negative marine bacteria: an update. Mar Drugs 5:85–112Google Scholar
  69. 69.
    Ovodov YS (2006) Bacterial capsular antigens. Structural patterns of capsular antigens. Biochemistry-Moscow 71:937–954Google Scholar
  70. 70.
    Schaffer C, Messner P (2005) The structure of secondary cell wall polymers: how Gram-positive bacteria stick their cell walls together. Microbiology 151:643–651Google Scholar
  71. 71.
    Nazarenko EL, Komandrova NA, Gorshkova RP, Tomshich SV, Zubkov VA, Kilcoyne M, Savage AV (2003) Structures of polysaccharides and oligosaccharides of some Gram-negative marine Proteobacteria. Carbohydr Res 338:2449–2457Google Scholar
  72. 72.
    Astronomo RD, Burton DR (2010) Carbohydrate vaccines: developing sweet solutions to sticky situations? Nat Rev 9:308–324Google Scholar
  73. 73.
    Pozsgay V (2008) Recent developments in synthetic oligosaccharide-based bacterial vaccines. Curr Top Med Chem 8:126–140Google Scholar
  74. 74.
    Jones C (2005) Vaccines based on the cell surface carbohydrates of pathogenic bacteria. Ann Acad Bras Cienc 77:293–324Google Scholar
  75. 75.
    Medgyes A, Bajza I, Farkas E, Pozsgay V, Liptak A (2000) Synthetic studies towards the O-specific polysaccharide of Shigella sonnei. J Carbohydr Chem 19:285–310Google Scholar
  76. 76.
    Toth A, Medgyes A, Bajza I, Liptak A, Batta G, Kontrohr T, Peterffy K, Pozsgay V (2000) Synthesis of the repeating unit of the O-specific polysaccharide of Shigella sonnei and quantitation of its serologic activity. Bioorg Med Chem Lett 10:19–21Google Scholar
  77. 77.
    Gyemant G, Toth A, Bajza I, Kandra L, Liptak A (2001) Identification and structural analysis of synthetic oligosaccharides of Shigella sonnei using MALDI-TOF MS. Carbohydr Res 334:315–322Google Scholar
  78. 78.
    Binns MW, Vaugham S, Timmis KN (1985) O-Antigens are essential virulance factors of Shigella sonnei and Shigella dysenteriae 1. ZBL Bakt Mik Hyg B 181:197–205Google Scholar
  79. 79.
    Wu X, Cui L, Lipinski T, Bundle DR (2010) Synthesis of monomeric and dimeric repeating units of zwitterionic type 1 capsular polysaccharide from Streptococcus pneumonia. Chem Eur J 16:3476–3488Google Scholar
  80. 80.
    Tzianabos AO, Wang JY, Kaspar DL (2003) Biological chemistry of immunomodulation by zwitterionic polysaccharides. Carbohydr Res 338:2531–2538Google Scholar
  81. 81.
    Dinkelaar J, De Jong AR, Van Meer R, Somers M, Lodder G, Overkleeft HS, Codée JDC, Van der Marel GA (2009) Stereodirecting effect of the pyranosyl C-5 substituent in glycosylation reactions. J Org Chem 74:4982–4991Google Scholar
  82. 82.
    Alpe M, Oscarson S (2003) Synthesis of tetra- and pentasaccharides corresponding to the capsular polysaccharide of Streptococcus pneumoniae type 9A&L, 9N and 9A. Carbohydr Res 338:2605–2609Google Scholar
  83. 83.
    Alpe M, Oscarson S (2002) Synthesis of oligosaccharides corresponding to Streptococcus pneumoniae type 9 capsular polysaccharide structures. Carbohydr Res 337:1715–1722Google Scholar
  84. 84.
    Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900Google Scholar
  85. 85.
    Yamamoto K, Watanabe N, Matsuda H, Oohara K, Araya T, Hashimoto M, Miyairi K, Okazaki I, Saito M, Shimizu T, Kato H, Okuno T (2005) Design, synthesis, and enzymatic property of a sulfur-substituted analogue of trigalacturonic acid. Bioorg Med Chem Lett 15:4932–4935Google Scholar
  86. 86.
    Magaud D, Grandjean C, Doutheau A, Anker D, Shevchik V, Cotte-Pattat N, Robert-Baudouy J (1998) Synthesis of the two monomethyl esters of the disaccharide 4-O-α-D-galacturonosyl-D-galacturonic acid and of precursors for the preparation of higher oligomers methyl uronated in definite sequences. Carbohydr Res 314:189–199Google Scholar
  87. 87.
    Magaud D, Grandjean C, Doutheau A, Anker D, Shevchik V, Cotte-Pattat N, Robert-Baudouy J (1997) An efficient and highly stereoselective α-(1→4) glycosylation between two D-galacturonic acid ester derivatives. Tetrahedron Lett 38:241–244Google Scholar
  88. 88.
    Magaud D, Dolmazon R, Anker D, Doutheau A, Dory YL, Deslongchamps P (2000) Differential reactivity of α- and β-anomers of glycosyl accepters in glycosylations. A remote consequence of the endo-anomeric effect? Org Lett 2:2275–2277Google Scholar
  89. 89.
    Codée JDC, De Jong AR, Dinkelaar J, Overkleeft HS, Van der Marel GA (2009) Stereoselectivity of glycosylations of conformationally restricted mannuronate esters. Tetrahedron 65:3780–3788Google Scholar
  90. 90.
    Clausen MH, Madsen R (2003) Synthesis of hexasaccharide fragments of pectin. Chem Eur J 9:3821–3832Google Scholar
  91. 91.
    Nemati N, Karapetyan G, Nolting B, Endress HU, Vogel C (2008) Synthesis of rhamnogalacturonan I fragments by a modular design principle. Carbohydr Res 343:1730–1742Google Scholar
  92. 92.
    Reiffarth D, Reimer KB (2008) Synthesis of two repeat units corresponding to the backbone of the pectic polysaccharide rhamnogalacturonan I. Carbohydr Res 343:179–188Google Scholar
  93. 93.
    Maruyama M, Takeda T, Shimizu N, Hada N, Yamada H (2000) Synthesis of a model compound related to an anti-ulcer pectic polysaccharide. Carbohydr Res 325:83–92Google Scholar
  94. 94.
    Scanlan EM, Mackeen MM, Wormald MR, Davis BG (2010) Synthesis and solution-phase conformation of the RG-I fragment of the plant polysaccharide pectin reveals a modification-modulated assembly mechanism. J Am Chem Soc. doi: 10.1021/ja9090963 Google Scholar
  95. 95.
    Chauvin AL, Nepogodiev SA, Field RA (2005) Synthesis of a 2,3,4-triglycosylated rhamnoside fragment of rhamnogalacturonan-II side chain a using a late stage oxidation approach. J Org Chem 70:960–966Google Scholar
  96. 96.
    Moe ST, Draget KI, Skjåk-Bræk G, Smidsrød O (1995) Food polysaccharides and their applications. Marcel Dekker, New YorkGoogle Scholar
  97. 97.
    Iwamoto M, Kurachi M, Nakashima T, Kim D, Yamaguchi K, Oda T, Iwamoto Y, Muramatsu T (2005) Structure–activity relationship of alginate oligosaccharides in the induction of cytokine production from RAW264.7 cells. FEBS Lett 579:4423–4429Google Scholar
  98. 98.
    Flo TH, Ryan L, Latz E, Takeuchi O, Monks BG, Lien E, Halaas Ø, Akira S, Skjåk-Bræk G, Golenbock DT, Espevik T (2002) Involvement of toll-like receptor (TLR) 2 and TLR4 in cell activation by mannuronic acid polymers. J Biol Chem 38:35489–35495Google Scholar
  99. 99.
    Codée JDC, Van den Bos LJ, De Jong AR, Dinkelaar J, Lodder G, Overkleeft HS, Van der Marel GA (2009) The stereodirecting effect of the glycosyl C5-carboxylate ester: stereoselective synthesis of β-mannuronic acid alginates. J Org Chem 74:38–47Google Scholar
  100. 100.
    van den Bos LJ, Dinkelaar J, Overkleeft HS, van der Marel GA (2006) Stereocontrolled synthesis of β-D-mannuronic acid esters: synthesis of an alginate trisaccharide. J Am Chem Soc 128:13066–13067Google Scholar
  101. 101.
    Jiang ZH, Xu RS, Wilson C, Brenk A (2007) Synthesis of β-1, 4-di-D-mannuronic acid glycosides as potential ligands for toll-like receptors. Tetrahedron Lett 48:2915–2918Google Scholar
  102. 102.
    Dinkelaar J, van den Bos LJ, Hogendorf WFJ, Lodder G, Overkleeft HS, Codee JDC, van der Marel GA (2008) Stereoselective synthesis of L-guluronic acid alginates. Chem Eur J 14:9400–9411Google Scholar
  103. 103.
    Chi FC, Kulkarni SS, Zulueta MML, Hung SC (2009) Synthesis of alginate oligosaccharides containing L-guluronic acids. Chem Asian J 4:386–390Google Scholar
  104. 104.
    Walvoort MTC, Lodder G, Mazurek J, Overkleeft HS, Codee JDC, van der Marel GA (2009) Equatorial anomeric triflates from mannuronic acid esters. J Am Chem Soc 131:12080–12081Google Scholar
  105. 105.
    Crich D (2002) Chemistry of glycosyl triflates: synthesis of β-mannosides. J Carbohydr Chem 21:667–690Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Jeroen D. C. Codée
    • 1
  • Alphert E. Christina
    • 1
  • Marthe T. C. Walvoort
    • 1
  • Herman S. Overkleeft
    • 1
  • Gijsbert A. van der Marel
    • 1
  1. 1.Leiden Institute of ChemistryLeiden UniversityLeidenThe Netherlands

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