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Short chain regioselectively hydrolyzed scleroglucans induce maturation of porcine dendritic cells

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Abstract

Branched β-1,3/1,6-glucans (scleroglucan) were produced by cultivation of Sclerotium rolfsii ATCC 15205. Regioselective hydrolysis at the β-1,3-linkage of the cell-free and purified polysaccharide was performed in borosilicate glass bottles at pH 5, 121°C, and 1 bar for 72 h. The mixture was divided into four molar mass fractions by stepwise cross-flow filtration using different cutoffs. In vitro studies revealed that scleroglucan hydrolysates with a low molar mass of less than 5 kDa significantly stimulated the activation and maturation of porcine monocyte derived dendritic cells (MoDC) by upregulation of CD40 and CD80/86 as well as by reduction of antigen uptake. MoDC treated with low molar mass scleroglucan showed a considerable increase in the amounts of secreted proinflammatory cytokine tumor necrosis factor alpha and stimulated the proliferation of lymphocytes. Therefore, scleroglucan molecules of low molecular weight are able to induce activation and maturation of porcine DC, which are key initiators of inflammatory and adaptive immune responses, and could provide improved protection against infectious diseases.

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References

  1. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18:767–811

  2. Bimczok D, Doll S, Rau H, Goyarts T, Wundrack N, Naumann M, Danicke S, Rothkotter HJ (2007a) The Fusarium toxin deoxynivalenol disrupts phenotype and function of monocyte-derived dendritic cells in vivo and in vitro. Immunobiology 212:655–666

  3. Bimczok D, Rau H, Wundrack N, Naumann M, Rothkotter HJ, McCullough K, Summerfield A (2007b) Cholera toxin promotes the generation of semi-mature porcine monocyte-derived dendritic cells that are unable to stimulate T cells. Vet Res 38:597–612

  4. Cao LZ, Lin ZB (2002) Regulation on maturation and function of dendritic cells by Ganoderma lucidum polysaccharides. Immunol Lett 83:163–169

  5. Carmona EM, Vassallo R, Vuk-Pavlovic Z, Standing JE, Kottom TJ, Limper AH (2006) Pneumocystis cell wall beta-glucans induce dendritic cell costimulatory molecule expression and inflammatory activation through a fas–fas ligand mechanism. J Immunol 177:459–467

  6. Carrasco CP, Rigden RC, Schaffner R, Gerber H, Neuhaus V, Inumaru S, Takamatsu H, Bertoni G, McCullough KC, Summerfield A (2001) Porcine dendritic cells generated in vitro: morphological, phenotypic and functional properties. Immunol 104:175–184

  7. Chen S-D, Hsieh M-C, Chiou M-T, Lai Y-S, Cheng Y-H (2008) Effects of fermentation products of Ganoderma lucidum on growth performance and immunocompetence in weanling pigs. Arch Anim Nutr 62:22–32

  8. Cox P, Buttiglione R (2003) Regulation (EC) No 1831/2003 of the European Parliament and of the Council. L268:29–43

  9. Dalmo RA, Bogwald J, Ingebrigtsen K, Seljelid R (1996) The immunomodulatory effect of Laminaran [β(1,3)-d-glucan] on Atlantic salmon, Salmo salar, anterior kidney leucocytes after intraperitoneal, peroral and peranal administration. J Fish Dis 19:449–457

  10. Dillon S, Agrawal S, Banerjee K, Letterio J, Denning TL, Oswald-Richter K, Kasprowicz DJ, Kellar K, Pare J, van Dyke T, Ziegler S, Unutmaz D, Pulendran B (2006) Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J Clin Invest 116:916–928

  11. Eicher SD, McKee CA, Carroll JA, Pajor EA (2006) Supplemental vitamin C and yeast cell wall β-glucan as growth enhancers in newborn pigs and as immunomodulators after an endotoxin challenge after weaning. J Anim Sci 84:2352–2360

  12. Gallucci S, Matzinger P (2001) Danger signals: SOS to the immune system. Curr Opin Immunol 13:114–119

  13. Gantner BN, Simmons RM, Canavera SJ, Akira S, Underhill DM (2003) Collaborative induction of inflammatory responses by dectin-1 and toll-like receptor 2. J Exp Med 197:1107–1117

  14. Giavasis I, Harvey LM, McNeil B (2005) Scleroglucan. In: Steinbüchel A, Doi Y (eds) Biotechnology of Biopolymers, vol 1. Wiley-VCH, Weinheim, pp 679–702

  15. Hahn TW, Lohakare JD, Lee SL, Moon WK, Chae BJ (2006) Effects of supplementation of β-glucans on growth performance, nutrient digestibility, and immunity in weanling pigs. J Anim Sci 84:1422–1428

  16. Hong F, Hansen RD, Yan J, Allendorf DJ, Baran JT, Ostroff GR, Ross GD (2003) β-Glucan functions as an adjuvant for monoclonal antibody immunotherapy by recruiting tumoricidal granulocytes as killer cells. Cancer Res 63:9023–9031

  17. Hong F, Yan J, Baran JT, Allendorf DJ, Hansen RD, Ostroff GR, Xing PX, Cheung N-KV, Ross GD (2004) Mechanism by which orally administered β-1,3-glucans enhance the tumoricidal activity of antitumor monoclonal antibodies in murine tumor models. J Immunol 173:797–806

  18. Huber K, Rau U, Maier T, Schilling B (2002) Scleroglucans and cosmetic compositions containing the new compounds. US 6369217

  19. Kikuchi T, Ohno N, Ohno T (2002) Maturation of dendritic cells induced by Candida β-d-glucan. Int Immunopharmacol 2:1503–1508

  20. Kishida E, Yoshiaki S, Misaki A (1992) Effects of branch distribution and chemicals modifications of antitumor (1-3)-β-d-glucans. Carbohydr Polymers 17:89–95

  21. Kojima T, Tabaka K, Ikumoto T, Yanaki T (1984) Depolymerization of Schizophyllan by controlled hydrodynamic shear. Agric Biol Chem 48:915–921

  22. Kulicke WM, Lettau AI, Thielking H (1997) Correlation between immunological activity, molar mass, and molecular structure of different 1,3-β-d-glucans. Carbohydr Res 297:135–143

  23. Lee HK, Iwasaki A (2007) Innate control of adaptive immunity: dendritic cells and beyond. Sem Immunol 19:48–55

  24. Li J, Li DF, Xing JJ, Cheng ZB, Lai CH (2006) Effects of β-glucan extracted from Saccharomyces cerevisiae on growth performance, and immunological and somatotropic responses of pigs challenged with Escherichia coli lipopolysaccharide. J Anim Sci 84:2374–2381

  25. Ljungman AG, Leanderson P, Tagesson C (1998) β-1,3-glucan stimulates nitric oxide generation and cytokine mRNA expression in macrophages. Environ Toxicol Phar 5:273–281

  26. Maier T, Rau U, Dieringer A (2003) Process for the production of scleroglucan. WO 03016545

  27. Mao XF, Piao XS, Lai CH, Li DF, Xing JJ, Shi BL (2005) Effects of β-glucan obtained from the Chinese herb Astragalus membranaceus and lipopolysaccharide challenge on performance, immunological, adrenal, and somatotropic responses of weanling pigs. J Anim Sci 83:2775–2782

  28. McIntosh M, Stone BA, Stanisich VA (2005) Curdlan and other bacterial 1,3-β-d-glucans. Appl Microbiol Biotechnol 68:163–173

  29. Mueller A, Raptis J, Rice PJ, Kalbfleisch JH, Stout RD, Ensley HE, Browder W, Williams DL (2000) The influence of glucan polymer structure and solution conformation on binding to (1–>3)-β-d-glucan receptors in a human monocyte-like cell line. Glycobiology 10:339–46

  30. Muenzberg J, Rau U, Wagner F (1995) Investigations to the regioselective hydrolysis of a branched β-1,3-glucan. Carbohydr Polymers 27:271–276

  31. Muller A, Rice PJ, Ensley HE, Coogan PS, Kalbfleish JH, Kelley JL, Love EJ, Portera CA, Ha T, Browder IW, Williams DL (1996) Receptor binding and internalization of a water-soluble (1–>3)-beta-d-glucan biologic response modifier in two monocyte/macrophage cell lines. J Immunol 156:3418–25

  32. Omarsdottir S, Olafsdottir ES, Freysdottir J (2006) Immunomodulating effects of lichen-derived polysaccharides on monocyte-derived dendritic cells. Int Immunopharmacol 6:1642–1650

  33. Park SK, Kim GY, Lim JY, Kwak JY, Bae YS, Lee JD, Oh YH, Ahn SC, Park YM (2003) Acidic polysaccharides isolated from Phellinus linteus induce phenotypic and functional maturation of murine dendritic cells. Biochem Biophys Res Commun 312:449–458

  34. Patra AK (2007) Nutritional management in organic livestock farming for improved ruminant health and production—an overview. Livest Res Rural Dev 19:41–42

  35. Pirri R, Huet Y, Donche A (1993) Process for enhancing oil recovery using scleroglucan powders. US 5323857

  36. Pretus HA, Ensley HE, McNamee RB, Jones EL, Browder IW, Williams DL (1991) Isolation, physicochemical characterization and preclinical efficacy evaluation of soluble scleroglucan. J Pharmacol Exp Ther 257:500–510

  37. Prokop A, Rapp P, Wagner F (1994) Production, purification, and characterization of an extracellular endo-beta-1,3-glucanase from a monokaryon of Schizophyllum commune ATCC 38548 defective in exo-beta-1,3-glucanase formation. Can J Microbiol 40:18–23

  38. Rapp P (1992) Formation, separation and characterization of three β-1,3-glucanases from Sclerotium glucanicum. Biochim Phys Acta 1117:7–14

  39. Rau U (2004) Glucans secreted by fungi. Turk Electron J Biotechnol 2:30–36

  40. Rau U (2005) Schizophyllan. In: Steinbüchel A, Doi Y (eds) Biotechnology of biopolymers, vol 1. Wiley-VCH, Weinheim, pp 703–735

  41. Rau U, Brandt C (1994) Oxygen controlled batch cultivations of Schizophyllum commune for enhanced production of branched β-1,3-glucans. Bioproc Biosys Eng 11:161–165

  42. Rau U, Müller RJ, Cordes K, Klein J (1990) Process and molecular data of branched 1,3-β-d-glucans in comparison with Xanthan. Bioproc Biosys Eng 5:89–93

  43. Rice PJ, Adams EL, Ozment-Skelton T, Gonzalez AJ, Goldman MP, Lockhart BE, Barker LA, Breuel KF, DePonti WK, Kalbfleisch JH, Ensley HE, Brown GD, Gordon S, Williams DL (2005) Oral delivery and gastrointestinal absorption of soluble glucans stimulate increased resistance to infectious challenge. J Pharmacol Exp Ther 314:1079–1086

  44. Rogers NC, Slack EC, Edwards AD, Nolte MA, Schulz O, Schweighoffer E, Williams DL, Gordon S, Tybulewicz VL, Brown GD, Reis E Sousa C (2005) Syk-dependent cytokine induction by dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22:507–517

  45. Sallusto F, Cella M, Danieli C, Lanzavecchia A (1995) Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med 182:389–400

  46. Schilling BM (2000) Sclerotium rolfsii ATCC 15205 in continuous culture: economical aspects of scleroglucan production. Bioproc Biosys Eng 22:57–61

  47. Schilling BM, Rau U, Maier T, Fankhauser P (1999) Modeling and scale-up of the unsterile scleroglucan production process with Sclerotium rolfsii ATCC 15205. Bioproc Biosys Eng 20:195–201

  48. Schilling BM, Henning A, Rau U (2000) Repression of oxalic acid biosynthesis in the unsterile scleroglucan production process with Sclerotium rolfsii ATCC 15205. Bioproc Biosys Eng 22:51–55

  49. Schmitz S (2004) Untersuchungen zur immunmodulativen Wirkung von β-1,3/1,6-Glukanen bei Schweinen. Ph.D. thesis, University of Veterinary Medicine Hannover, Hannover

  50. Somogyi MA (1952) Notes on sugar determination. Biol Chem 195:19–23

  51. Steinman RM, Banchereau J (2007) Taking dendritic cells into medicine. Nature 449:419–426

  52. Suda M, Ohno N, Adachi Y, Yadomae T (1994) Preparation and properties of metabolically 3H- or 13C-labeled 1,3-β-d-glucan SSG from Sclerotinia sclerotiorum IFO 9395. Carbohydr Res 254:213–220

  53. Survase SA, Saudagar PS, Singhal RS (2007) Use of complex media for the production of scleroglucan by Sclerotium rolfsii MTCC 2156. Bioresour Technol 98:1509–1512

  54. Uchi H, Arrighi JF, Aubry JP, Furue M, Hauser C (2002) The sesquiterpene lactone parthenolide inhibits LPS- but not TNF-a-induced maturation of human monocyte-derived dendritic cells by inhibition of the p38 mitogen-activated protein kinase pathway. J Allergy Clin Immunol 110:269–276

  55. Wang Z, Guo Y, Yuan J, Zhang B (2008) Effect of dietary β-1,3/1,6-glucan supplementation on growth performance, immune response and plasma prostaglandin E2, growth hormone and ghrelin in weanling piglets. Asian Austral J Anim Sci 21:707–714

  56. Zhang M, Cheung PCK, Zhang L, Chiu C-M, Ooi VEC (2004) Carboxymethylated β-glucans from mushroom sclerotium of Pleurotus tuber-regium as novel water-soluble anti-tumor agent. Carbohydr Polymers 57:319–325

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Acknowledgments

The study was kindly supported by the Federal Ministry of Food, Agriculture and Consumer Protection managed by the Federal Institute of Agriculture and Food (grant 05HS010) and by the EU, 6th framework program “Feed for Pig Health”, FOOD-CT 2004-506144.

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Correspondence to Udo Rau.

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Bimczok, D., Wrenger, J., Schirrmann, T. et al. Short chain regioselectively hydrolyzed scleroglucans induce maturation of porcine dendritic cells. Appl Microbiol Biotechnol 82, 321–331 (2009). https://doi.org/10.1007/s00253-008-1813-7

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Keywords

  • Porcine dendritic cells
  • Cytokines
  • β-Glucan
  • Scleroglucan
  • Regioselective hydrolysis