Mechanism of mild acid hydrolysis of galactan polysaccharides with highly ordered disaccharide repeats leading to a complete series of exclusively odd-numbered oligosaccharides

FEBS Journal

Volumn 276, Issue 7, 2009, Pages 2125-2137

  Yang, Bo ^a   Yu, Guangli ^a   Zhao, Xia ^a   Jiao, Guangling ^a   Ren, Sumei ^a   Chai, Wengang ^a,b  

^a OCEAN UNIVERSITY OF CHINA   (China)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Acid hydrolysis; Agarose; Carrageenan; Mass spectrometry; Polysaccharide

Indexed keywords

CARRAGEENAN; OLIGOSACCHARIDE;

ARTICLE; CHEMICAL BOND; DEGRADATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; MASS SPECTROMETRY; PRIORITY JOURNAL; REDUCTION; SEQUENCE ANALYSIS;

CARBOHYDRATE SEQUENCE; CARRAGEENAN; DISACCHARIDES; GALACTANS; HYDROLYSIS; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; POLYSACCHARIDES; SULFATES; TANDEM MASS SPECTROMETRY;

EID: 62149105066     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.06947.x     Document Type: Article

References (41)

1. Mourao PA Pereira MS (1999) Searching for alternatives to heparin: sulfated fucans from marine invertebrates. Trends Cardiovasc Med 9, 225 232.
2. McCarthy B (2007) Antivirals - an increasingly healthy investment. Nat Biotechnol 25, 1390 1393.
3. Baker B, Zambryski P, Staskawicz B Dinesh-Kumar SP (1997) Signaling in plant-microbe interactions. Science 276, 726 733.
4. Potin P, Bouarab K, Salaun JP, Pohnert G Kloareg B (2002) Biotic interactions of marine algae. Curr Opin Plant Biol 5, 308 317.
5. Carlucci MJ, Scolaro LA, Noseda MD, Cerezo AS Damonte EB (2004) Protective effect of a natural carrageenan on genital herpes simplex virus infection in mice. Antiviral Res 64, 137 141.
6. Damonte EB, Matulewicz MC Cerezo AS (2004) Sulfated seaweed polysaccharides as antiviral agents. Curr Med Chem 11, 2399 2419.
7. Buck CB, Thompson CD, Roberts JN, Muller M, Lowy DR Schiller JT (2006) Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathog 2, 671 680.
8. Roberts JN, Buck CB, Thompson CD, Kines R, Bernardo M, Choyke PL, Lowy DR Schiller JT (2007) Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat Med 13, 857 861.
9. De Ruiter GA Rudolph B (1997) Carrageenan biotechnology. Trends Food Sci Technol 8, 389 395.
10. Barbeyron T, Gerard A, Potin P, Henrissat B Kloareg B (1998) The kappa-carrageenase of the marine bacterium Cytophaga drobachiensis. Structural and phylogenetic relationships within family-16 glycoside hydrolases. Mol Biol Evol 15, 528 537.
11. Allouch J, Jam M, Helbert W, Barbeyron T, Kloareg B, Henrissat B Czjzek M (2003) The three-dimensional structures of two beta-agarases. J Biol Chem 278, 47171 47180.
12. Michel G, Chantalat L, Fanchon E, Henrissat B, Kloareg B Dideberg O (2001) The iota-carrageenase of Alteromonas fortis. A beta-helix fold-containing enzyme for the degradation of a highly polyanionic polysaccharide. J Biol Chem 276, 40202 40209.
13. Ma C, Lu X, Shi C, Li J, Gu Y, Ma Y, Chu Y, Han F, Gong Q Yu W (2007) Molecular cloning and characterization of a novel beta-agarase, AgaB, from marine Pseudoalteromonas sp. CY24. J Biol Chem 282, 3747 3754.
14. Guibet M, Colin S, Barbeyron T, Genicot S, Kloareg B, Michel G Helbert W (2007) Degradation of lambda-carrageenan by Pseudoalteromonas carrageenovora lambda-carrageenase: a new family of glycoside hydrolases unrelated to kappa- and iota-carrageenases. Biochem J 404, 105 114.
15. Caram-Lelham N (1995) Preparative sepatarion of oligosaccharides from κ-carrageenan, sodium hyaluronate and dextran by Superdex30 prep. grade. Carbohydr Res 273, 71 76.
16. Chen HM, Zheng L, Lin W Yan XJ (2004) Product monitoring and quantitation of oligosaccharides composition in agar hydrolysates by precolumn labeling HPLC. Talanta 64, 773 777.
17. Chen HM Yan XJ (2005) Antioxidant activities of agaro-oligosaccharides with different degrees of polymerization in cell-based system. Biochim Biophys Acta 1722, 103 111.
18. Clingman AL, Num JR Stephen AM (1957) Red-seaweed Polysacchurides. J Chem Soc, 197 203.
19. Peat S, Turvey JR Rees DA (1961) Carbohydrates of the red alga Porphyra umbilicalis. J Chem Soc, 1590 1595.
20. Kazlowski B, Pan CL Ko YT (2008) Separation and quantification of neoagaro- and agaro-oligosaccharide products generated from agarose digestion by beta-agarase and HCl in liquid chromatography systems. Carbohydr Res 343, 2443 2450.
21. Yu G, Guan H, Ioanoviciu AS, Sikkander SA, Thanawiroon C, Tobacman JK, Toida T Linhardt RJ (2002) Structural studies on kappa-carrageenan derived oligosaccharides. Carbohydr Res 337, 433 440.
22. Yu G, Zhao X, Yang B, Ren S, Guan H, Zhang Y, Lawson AM Chai W (2006) Sequence determination of sulfated carrageenan-derived oligosaccharides by high-sensitivity negative-ion electrospray tandem mass spectrometry. Anal Chem 78, 8499 8505.
23. Zhang Z, Yu G, Zhao X, Liu H, Guan H, Lawson AM Chai W (2006) Sequence analysis of alginate-derived oligosaccharides by negative-ion electrospray tandem mass spectrometry. J Am Soc Mass Spectrom 17, 621 630.
24. Araki C Hirase S (1953) Studies on the chemical constitution of agar-agar. Exhaustive mercaptolyses of agar-agar. Bull Chem Soc Jpn 26, 463 467.
25. Stevenson TT Furneaux RH (1991) Chemical methods for the analysis of sulphated galactans from red algae. Carbohydr Res 210, 277 298.
26. Jol CN, Neiss TG, Penninkhof B, Rudolph B De Ruiter GA (1999) A novel high-performance anion-exchange chromatographic method for the analysis of carrageenans and agars containing 3,6-anhydrogalactose. Anal Biochem 268, 213 222.
27. Hama Y, Nakagawa H, Kurosawa M, Sumi T, Xia X Yamaguchi K (1998) A gas chromatographic method for the sugar analysis of 3,6-anhydrogalactose-containing algal galactans. Anal Biochem 265, 42 48.
28. Hama Y, Nakagawa H, Mochizuki K, Sumi T Hatate H (1999) Quantitative anhydrous mercaptolysis of algal galactans followed by HPLC of component sugars. J Biochem 125, 160 165.
29. Quemener B Lahaye M (1998) Comparative analysis of sulfated galactans from red algae by reductive hydrolysis and mild methanolysis coupled to two different HPLC techniques. J Appl Phycol 10, 75 81.
30. Goncalves AG, Ducatti DRB, Paranha RG, Eugenia M, Duarte R Noseda MD (2005) Positional isomers of sulfated oligosaccharides obtained from agarans and carrageenans: preparation and capillary electrophoresis separation. Carbohydr Res 340, 2123 2134.
31. Quemener B, Lahaye M Metro F (1995) Assessment of methanolysis for the determination of composite sugars of gelling carrageenans and agarose by HPLC. Carbohydr Res 266, 53 64.
32. Goncalves AG, Ducatti DR, Duarte ME Noseda MD (2002) Sulfated and pyruvylated disaccharide alditols obtained from a red seaweed galactan: ESIMS and NMR approaches. Carbohydr Res 337, 2443 2453.
33. Zhang Z, Xie J, Zhang F Linhardt RJ (2007) Thin-layer chromatography for the analysis of glycosaminoglycan oligosaccharides. Anal Biochem 371, 118 120.
34. Edens RE, al-Hakim A, Weiler JM, Rethwisch DG, Fareed J Linhardt RJ (1992) Gradient polyacrylamide gel electrophoresis for determination of molecular weights of heparin preparations and low-molecular-weight heparin derivatives. J Pharm Sci 81, 823 827.
35. Chi L, Wolff JJ, Laremore TN, Restaino OF, Xie J, Schiraldi C, Toida T, Amster IJ Linhardt RJ (2008) Structural analysis of bikunin glycosaminoglycan. J Am Chem Soc 130, 2617 2625.
36. Palmarola-Adrados B, Juhasz T, Galbe M Zacchi G (2004) Hydrolysis of nonstarch carbohydrates of wheat-starch effluent for ethanol production. Biotechnol Prog 20, 474 479.
37. Jun M, Shao Y, Ho CT, Koetter U Lech S (2003) Structural identification of nonvolatile dimerization products of glucosamine by gas chromatography-mass spectrometry, liquid chromatography-mass spectrometry, and nuclear magnetic resonance analysis. J Agric Food Chem 51, 6340 6346.
38. Kolender AA Matulewicz MC (2002) Sulfated polysaccharides from the red seaweed Georgiella confluens. Carbohydr Res 337, 57 68.
39. Kolender AA Matulewicz MC (2004) Desulfation of sulfated galactans with chlorotrimethylsilane. Characterization of beta-carrageenan by 1H NMR spectroscopy. Carbohydr Res 339, 1619 1629.
40. Ciucanu I Costello CE (2003) Elimination of oxidative degradation during the per-O-methylation of carbohydrates. J Am Chem Soc 125, 16213 16219.
41. Chai W, Luo J, Lim CK Lawson AM (1998) Characterization of heparin oligosaccharide mixtures as ammonium salts using electrospray mass spectrometry. Anal Chem 70, 2060 2066.