Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Chemical Modification of Botryosphaeran: Structural Characterization and Anticoagulant Activity of a Water-Soluble Sulfonated ($1{\rightarrow}3$)($1{\rightarrow}6$)-${\beta}$-D-Glucan

  • Brandi, Jamile (Departamento de Fisica, Quimica e Biologia, Faculdade de Ciencias e Technologia, Universidade Estadual Paulista) ;
  • Oliveira, Eder C. (Departamento de Fisica, Quimica e Biologia, Faculdade de Ciencias e Technologia, Universidade Estadual Paulista) ;
  • Monteiro, Nilson K. (Departamento de Fisica, Quimica e Biologia, Faculdade de Ciencias e Technologia, Universidade Estadual Paulista) ;
  • Vasconcelos, Ana Flora D. (Departamento de Fisica, Quimica e Biologia, Faculdade de Ciencias e Technologia, Universidade Estadual Paulista) ;
  • Dekker, Robert F.H. (Biorefining Research Institute, Lakehead University) ;
  • Barbosa, Aneli M. (Departamento de Bioquimica e Biotechnologia, Universidade Estadual de Londrina) ;
  • Silveira, Joana L.M. (Departamento de Bioquimica e Biologia Molecular, Universidade Federal do Parana) ;
  • Mourao, Paulo A.S. (Laboratorio de Tecido Conjuntivo, H. U. Clementino Fraga Filho, Universidade Federal do Rio de Janeiro) ;
  • Silva, Maria De Lourdes Corradi Da (Departamento de Fisica, Quimica e Biologia, Faculdade de Ciencias e Technologia, Universidade Estadual Paulista)
  • Received : 2011.05.13
  • Accepted : 2011.06.29
  • Published : 2011.10.28
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Abstract

The exopolysaccharide botryosphaeran ($EPS_{GLC}$; a ($1{\rightarrow}3$)($1{\rightarrow}6$)-${\beta}$-D-glucan from Botryosphaeria rhodina MAMB-05) was sulfonated to produce a water-soluble fraction ($EPS_{GLC}$-S) using pyridine and chlorosulfonic acid in formamid. This procedure was then repeated twice to produce another fraction ($EPS_{GLC}$-RS) with a higher degree of substitution (DS, 1.64). The purity of each botryosphaeran sample (unsulfonated and sulfonated) was assessed by gel filtration chromatography (Sepharose CL-4B), where each polysaccharide was eluted as a single symmetrical peak. The structures of the sulfonated and re-sulfonated botryosphaerans were investigated using ultraviolet-visible (UV-Vis), Fourier-transform infrared (FT-IR), and $^{13}C$ nuclear magnetic resonance ($^{13}C$ NMR) spectroscopies. $EPS_{GLC}$ and $EPS_{GLC}$-RS were also assayed for anticoagulation activity, and $EPS_{GLC}$-RS was identified as an anticoagulant.

Keywords

References

  1. Alban, S., A. Schauerte, and G. Franz. 2002. Anticoagulant sulfated polysaccharides: Part I. Synthesis and structure-activity relationships of new pullulan sulfates. Carbohydr. Polym. 47: 267-276. https://doi.org/10.1016/S0144-8617(01)00178-3
  2. Alban, S. and G. Franz. 2000. Characterization of the anticoagulant actions of a semisynthetic curdlan sulfate. Thromb. Res. 99: 377-388. https://doi.org/10.1016/S0049-3848(00)00264-4
  3. Alban, S., W. Jeske, D. Welzel, G. Franz, and J. Fareed. 1995. Anticoagulant and antithrombotic actions of a semisynthetic $\beta$- 1,3-glucan sulfate. Thromb. Res. 78: 201-210. https://doi.org/10.1016/0049-3848(95)00049-W
  4. Barbosa, A. M., R. M. Steluti, R. F. H. Dekker, M. S. Cardoso, and M. L. Corradi da Silva. 2003. Structural characterization of botryosphaeran: A $\beta$-(1$\rightarrow$3;1$\rightarrow$6)-D-glucan produced by the ascomyceteous fungus, Botryosphaeria sp. Carbohydr. Res. 338: 1691-1698. https://doi.org/10.1016/S0008-6215(03)00240-4
  5. Bradford, M. M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  6. Chan, G. C. F., W. K Chan, and D. M. Y. Sze. 2009. The effects of $\beta-glucan$ on human immune and cancer cells. J. Hematol. Oncol. 2: 1-11. https://doi.org/10.1186/1756-8722-2-1
  7. Chen, J. and R. Seviour. 2007. Medicinal importance of fungal $\beta$-(1$\rightarrow$3),(1$\rightarrow$6)-glucans. Mycol. Res. 111: 635-652. https://doi.org/10.1016/j.mycres.2007.02.011
  8. Corradi da Silva, M. L., N. L. Izeli, P. F. Martinez, I. R. Silva, C. J. L. Constantino, M. S. Cardoso, et al. 2005. Purification and structural characterisation of $\beta$-(1$\rightarrow$3;1$\rightarrow$6)$-_D-glucan$ (botryosphaerans) from Botryosphaeria rhodina grown on sucrose and fructose as carbon sources: A comparative study. Carbohydr. Polym. 61: 10-17. https://doi.org/10.1016/j.carbpol.2005.01.002
  9. Dekker, R. F. H. and A. M. Barbosa. 2001. The effects of aeration and veratryl alcohol on the production of two laccases by the ascomycete Botryosphaeria sp. Enz. Microb. Technol. 28: 81-88. https://doi.org/10.1016/S0141-0229(00)00274-X
  10. Dubois, M., K. A. Gilles, J. K. Hamilton, P. A. Rebers, and F. Smith. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28: 353-356.
  11. Giese, E. C., L. G. Covizzi, R. F. H. Dekker, N. K. Monteiro, M. L. Corradi da Silva, and A. M. Barbosa. 2006. Enzymatic hydrolysis of botryosphaeran and laminarin by $\beta$-1,3-glucanases produced by Botryosphaeria rhodina and Trichoderma harzianum Rifai. Process Biochem. 41: 1265-1271. https://doi.org/10.1016/j.procbio.2005.12.023
  12. Gracher, A. H., T. R. Cipriani, E. R. Carbonero, P. A. J. Gorin, and M. Iacomini. 2010. Antithrombin and heparin cofactor II-mediated inactivation of $\alpha$-thrombin by a synthetic, sulfated mannogalactan. Thromb. Res. 126: e180-e187. https://doi.org/10.1016/j.thromres.2010.04.008
  13. Han, F., W. Yao, X. Yang, X Liu, and X. Gao. 2005. Experimental study on anticoagulant and antiplatelet aggregation activity of a chemically sulfated marine polysaccharide YCP. Int. J. Biol. Macromol. 36: 201-207. https://doi.org/10.1016/j.ijbiomac.2005.06.003
  14. Jouault, S. C., L. Chevolot, D. Helley, J. Ratiskol, A. Bros, C. Sinquin, et al. 2001. Characterization, chemical modifications and in vitro anticoagulant properties of an exopolysaccharide produced by Alteromonas infernus. Biochim. Biophys. Acta 1528: 141-151. https://doi.org/10.1016/S0304-4165(01)00185-4
  15. Kery, V., G. Kogan, Z. Zajakova, L. Masler, and J. Alfoldi. 1991. Hydrolysis of yeast cell-wall glucan by extracellular (1$\rightarrow$3)-$\beta$-glucanases from Aspergillus niger. Enz. Microb. Technol. 13: 87-90. https://doi.org/10.1016/0141-0229(91)90194-F
  16. Leung, M. Y. K., C. Liu, J. C. M. Koon, and K. P Fung. 2006. Polysaccharide biological response modifiers. Immunol. Lett. 105: 101-114. https://doi.org/10.1016/j.imlet.2006.01.009
  17. Lin, Y., L. Zhang, L. Chen, Y. Jin, F. Zeng, J. Jin, et al. 2004. Molecular mass and antitumor activities of sulfated derivatives of $\alpha$-glucan from Poria cocos mycelia. Int. J. Biol. Macromol. 34: 231-236. https://doi.org/10.1016/j.ijbiomac.2004.08.001
  18. Lu, T. Y., H. Nakashima, M. Premathan, R. Aragaki, T. Mimura, Y. Kaneko, N. Yamamoto, T. Miyakoshi, and T. R. Uryu. 2000. Specific biological activities of Chinese lacquer polysaccharides. Carbohydr. Polym. 43: 47-54. https://doi.org/10.1016/S0144-8617(99)00198-8
  19. Mahner, C., M. D. Lechmer, and E. Nordmeier. 2001. Synthesis and characterisation of dextran and pullulan sulphate. Carbohydr. Res. 331: 203-208. https://doi.org/10.1016/S0008-6215(00)00315-3
  20. Martinichen-Herrero, J. C., E. R. Carbonero, P. A. J. Gorin, and M. Iacomini. 2005. Anticoagulant and antithrombotic activity of a sulfate obtained from a glucan component of the lichen Parmotrema mantiqueirense Hale. Carbohydr. Polym. 60: 7-13. https://doi.org/10.1016/j.carbpol.2004.11.014
  21. Melo, F. R., M. S. Pereira, F. Foguel, and P. A. S. Mourao. 2004. Antithrombin-mediated anticoagulant activity of sulfated polysaccharides. J. Biol. Chem. 279: 20824-20835. https://doi.org/10.1074/jbc.M308688200
  22. Melo, M. R. S., J. P. A. Feitosa, A. L. P. Freitas, and R. C. M. Paula. 2002. Isolation and characterization of soluble sulfated polysaccharide from the red seaweed Gracilaria cornea. Carbohydr. Polym. 49: 491-498. https://doi.org/10.1016/S0144-8617(02)00006-1
  23. Mendes, S. F., O. Santos Jr., A. M. Barbosa, A. F. D. Vasconcelos, G. Aranda-Selverio, N. Monteiro, et al. 2009. Sulfonation and anticoagulant activity of botryosphaeran from Botryosphaeria rhodina MAMB-05 grown on fructose. Int. J. Biol. Macromol. 45: 305-309. https://doi.org/10.1016/j.ijbiomac.2009.06.004
  24. Miranda, C. C. B. O., R. F. H. Dekker, E. A. I. Fonseca, J. M. Serpeloni, I. M. S. Colus, and A. M. Barbosa. 2008. Anticlastogenic activity exhibited by botryosphaeran, a new exopolysaccharide produced by Botryosphaeria rhodina MAMB-05. Int. J. Biol. Macromol. 42: 172-177. https://doi.org/10.1016/j.ijbiomac.2007.10.010
  25. Miranda, C. C. B. O., R. F .H. Dekker, I. Colus, C. T. Zaia, I. Castro, and A. M. Barbosa. 2007. Botryosphaeran: A new fungal exopolysaccharide presenting antimutagenic, hypoglycaemic and hypocholesterolaemic activities in mice and rats. J. Biotechnol. 131S: S58-S64.
  26. O'Neill, A. N. 1955. Sulphated derivatives of laminarin. Can. J. Chem. 33: 1097-1101. https://doi.org/10.1139/v55-127
  27. Rice, P. J., P. E. Lockhart, L. A. Barker, E. L. Adams, H. E. Ensley, and D. L Williams. 2004. Pharmacokinetics of fungal $(1-3)-\beta-_D-glucans$ following intravenous administration in rats. Int. Immunopharmacol. 4: 1209-1215. https://doi.org/10.1016/j.intimp.2004.05.013
  28. Soeda, S., T. Kozako, K. Iwata, and H. Shimeno. 2000. Oversulfated fucoidan inhibits the basic fibroblast growth factor-induced tube formation by human umbilical vein endothelial cells: Its possible mechanism of action. Biochim. Biophys. Acta 1497: 127-134. https://doi.org/10.1016/S0167-4889(00)00052-5
  29. Soltanian, S., E. Stuyven, E. Cox, P. Sorgeloos, and P. Bossier. 2009. Beta-glucans as immunostimulant in vertebrates and invertebrates. Crit. Rev. Microbiol. 35: 109-138. https://doi.org/10.1080/10408410902753746
  30. Steluti, R. M., E. C. Giese, M. M. Piggato, A. F. G. Sumeija, L G. Covizzi, A. E. Job, et al. 2004. Comparison of botryosphaeran production by the ascomyceteous fungus Botryosphaeria sp., grown on different carbohydrate carbon sources, and their partial structural features. J. Basic Microbiol. 44: 480-486. https://doi.org/10.1002/jobm.200410415
  31. Surenjav, U., L. Zhang, X. Xu, X. Zhang, and F. Zeng. 2006. Effects of molecular structure on antitumor activities of (1$\rightarrow$3)$-\beta-_D-glucans$ from different Lentinus edodes. Carbohydr. Polym. 63: 97-104. https://doi.org/10.1016/j.carbpol.2005.08.011
  32. Vetvicka, V. and J.-C. Yvin. 2004. Effects of marine $\beta$-1,3 glucan on immune reactions. Int. Immunopharmacol. 4: 721-730. https://doi.org/10.1016/j.intimp.2004.02.007
  33. Wang, M. Z., L. Li, B. S. Zheng, N. Normakhamatov, and S. Y. Guo. 2007. Preparation and anticoagulation activity of sodium cellulose sulfate. Int. J. Biol. Macromol. 41: 376-382. https://doi.org/10.1016/j.ijbiomac.2007.05.007
  34. Whistler, R. L. and W. W. Spencer. 1964. Sulfation, pp. 235-275. In R. L. Whistler (ed.). Methods in Carbohydrate Chemistry (Vol 4). Academic Press, New York.
  35. Yang, J., Y. Du, R. Huang, Y. Wan, and Y. Wen. 2005. The structure-anticoagulant activity relationships of sulfated lacquer polysaccharide. Effect of carboxyl group and position of sulfation. Int. J. Biol. Macromol. 36: 9-15. https://doi.org/10.1016/j.ijbiomac.2005.03.002
  36. Yang, J., Y. Du, Y. Wen, T. Li, and L. Hu. 2003. Sulfation of Chinese lacquer polysaccharides in different solvents. Carbohydr. Polym. 52: 397-403. https://doi.org/10.1016/S0144-8617(02)00330-2
  37. Yoon, S. J., M. S. Pereira, M. S. G. Pavao, J. K. Hwang, Y. R. Pyun, and P. A. S. Mourao. 2002. The medicinal plant Porana volubilis contains polysaccharides with anticoagulant activity mediated by heparin cofactor II. Thromb. Res. 106: 51-58. https://doi.org/10.1016/S0049-3848(02)00071-3

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