Barley β-glucans-containing food enhances probiotic performances of beneficial bacteria

International Journal of Molecular Sciences

Volumn 15, Issue 2, 2014, Pages 3025-3039

  Arena, Mattia P ^a   Caggianiello, Graziano ^a   Fiocco, Daniela ^a   Russo, Pasquale ^a   Torelli, Michele ^b   Spano, Giuseppe ^a   Capozzi, Vittorio ^a  

^a UNIVERSITY OF FOGGIA   (Italy)

^b Department of Clinical and Experimental medicine University of Foggia ^*  (Italy)

Author keywords

Barley glucans; Lactobacillus; Pasta; Prebiotics; Probiotics

Indexed keywords

BETA GLUCAN; PROBIOTIC AGENT;

ARTICLE; BACTERIAL GROWTH; BARLEY; CELL ADHESION ASSAY; CELL SURVIVAL; COLONY FORMING UNIT; CONTROLLED STUDY; DIET; GASTROINTESTINAL TRANSIT; HUMAN; HUMAN CELL; INTESTINE CELL; LACTOBACILLUS; NONHUMAN; OPTICAL DENSITY; PASTA; CACO 2 CELL LINE; CELL ADHESION; CEREAL; CHEMISTRY; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

BETA-GLUCANS; CACO-2 CELLS; CELL ADHESION; CEREALS; HUMANS; LACTOBACILLUS; PROBIOTICS;

EID: 84894266318     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15023025     Document Type: Article

References (52)

1. Lam, K.L.; Cheung, C.K. Non-digestible long chainbeta-glucans as novel prebiotics. Bioact. Carbohydr. Diet. Fibers 2013, 2, 45-64.
2. Collado, M.C.; Isolauri, E.; Salminen, S.; Sanz, Y. The impact of probiotic on gut health. Curr. Drug Metab. 2009, 10, 68-78.
3. Schrezenmeir, J.; de Vrese, M. Probiotics, prebiotics, and synbiotics-approaching a definition. Am. J. Clin. Nutr. 2001, 73, 361S-364S.
4. Food and Agriculture Organization of United Nations and World Health Organization Working Group (FAO/WHO). Guidelines for the Evaluation of Probiotics in Food; Technical report for FAO/WHO: London, UK, 2002.
5. Vasilijevic, T.; Shah, N.P. Fermented Milk: Health Benefits beyond Probiotic Effect. In Handbook of Food Products Manufacturing; John Wiley & Sons, Inc.: Hoboken, NJ, USA; 2007; Volume 2, pp. 99-116.
6. Mayo, B.; van Sinderen, D.; Ventura, M. Genome analysis of food grade lactic acid-producing bacteria: From basics to applications. Curr. Genomics 2008, 9, 169-183.
7. Roberfroid, M.; Gibson, G.R.; Hoyles, L.; McCartney, A.L.; Rastall, R.; Rowland, I.; Wolvers, D.; Watzl, B.; Szajewska, H.; Stahl, B.; et al. Prebiotic effects: Metabolic and health benefits. Br. J. Nutr. 2010, 104, 1S-63S.
8. Blaut, M. Relationship of prebiotics and food to intestinal microflora. Eur. J. Nutr. 2002, 1, i11-i16.
9. Dass, N.B.; John, A.K.; Bassil, A.K.; Crumbley, C.W.; Shehee, W.R.; Maurio, F.P.; Moore, G.B.T.; Taylor, C.M.; Sanger, G.J. The relationship between the effects of short-chain fatty acids on intestinal motility in vitro and GPR43 receptor activation. Neurogastroenterol. Motil. 2007, 19, 66-74.
10. Xiong, Y.; Miyamoto, N.; Shibata, K.; Valasek, M.A.; Motoike, T.; Kedzierski, R.M.; Yanagisawa, M. Short-chain fatty acids stimulate leptin production in adipocytes through the G protein-coupled receptor GPR41. Proc. Natl. Acad. Sci. USA 2004, 101, 1045-1050.
11. Williams, E.A.; Coxhead, J.M.; Mathers, J.C. Anti-cancer effects of butyrate: use of micro-array technology to investigate mechanisms. Proc. Nutr. Soc. 2003, 62, 107-115.
12. Scheppach, W. Treatment of distal ulcerative colitis with short-chain fatty acid enemas a placebo-controlled trial. Dig. Dis. Sci. 1996, 41, 2254-2259.
13. Artis, D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 2008, 8, 411-420.
14. Nilsson, N.E.; Kotarsky, K.; Owman, C.; Olde, B. Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and activated by short-chain fatty acids. Biochem. Biophys. Res. Commun. 2003, 303, 1047-1052.
15. Le Poul, E.; Loison, C.; Struyf, S.; Springael, J.-Y.; Lannoy, V.; Decobecq, M.-E.; Brezillon, S.; Dupriez, V.; Vassart, G.; van Damme, J.; et al. Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation. J. Biol. Chem. 2003, 278, 25481-25489.
16. Topping, D.L.; Clifton, P.M. Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides. Physiol. Rev. 2001, 81, 1031-1064.
17. Lupton, J. Microbial degradation products influence colon cancer risk: The butyrate controversy. J. Nutr. 2004, 134, 479-482.
18. Macfarlane, G.T.; Gibson, G.R.; Cummings, J.H. Comparison of fermentation reactions in different regions of the human colon. J. Appl. Microbiol. 1992, 72, 57-64.
19. Holtekjølen, A.K.; Uhlen, A.K.; Bråthen, E.; Sahlstrøm, S.; Knutsen, S.H. Contents of starch and non-starch polysaccharides in barley varieties of different origin. Food Chem. 2006, 94, 348-358.
20. El Khoury, D.; Cuda, C.; Luhovyy, B.L.; Anderson, G.H. Beta Glucan: Health benefits in obesity and metabolic syndrome. J. Nutr. Metab. 2012, 2012, 851362.
21. Barsanti, L.; Passarelli, V.; Evangelista, V.; Frassanito, A.M.; Gualtieri, P. Chemistry, physico-chemistry and applications linked to biological activities of β-glucans. Nat. Prod. Rep. 2011, 28, 457-466.
22. Synytsya, A.; Novák, M. Structural diversity of fungal glucans. Carbohydr. Polym. 2013, 92, 792-809.
23. Godfrey, C.; Wing, C.; Daniel, S. The effects of β-glucan on human immune and cancer cells. J. Hematol. Oncol. 2009, 2, 25.
24. Murphy, E.A.; Davis, J.M.; Brown, A.S.; Carmichael, M.D.; Carson, J.A.; van Rooijen, N.; Ghaffar, A.; Mayer, E.P. Benefits of oat β-glucan on respiratory infection following exercise stress: Role of lung macrophages. Am. J. Physiol. 2008, 294, R1593-R1599.
25. Volman, J.J.; Mensink, R.P.; Ramakers, J.D.; de Winther, M.P.; Carlsen, H.; Blomhoff, R.; Buurman, W.A.; Plat, J. Dietary (1.3), (1.4)-β-D-glucans from oat activate nuclear factor-kappa B in intestinal leukocytes and enterocytes from mice. Nutr. Res. 2010, 30, 40-48.
26. Slavin, J.L. Dietary fiber and body weight. Nutrition 2005, 21, 411-418.
27. Jensen, M.K.; Koh-Banerjee, B.; Hu, F.B.; Franz, M.; Sampson, L.; Grønbæk, M.; Rimm, E.B. Intakes of whole grains, bran, and germ and the risk of coronary heart disease in men. Am. J. Clin. Nutr. 2004, 80, 1492-1499.
28. Brennan, C.S. Dietary fibre, glycaemic response, and diabetes. Mol. Nutr. Food Res. 2005, 49, 560-570.
29. Önning, G.; Wallmark, A.; Persson, M.; Åkesson, B.; Elmståhl, S.; Öste, R. Consumption of oat milk for 5 weeks lowers serum cholesterol and LDL cholesterol in freeliving men with moderate hypercholesterolemia. Ann. Nutr. Metab. 1999, 43, 301-309.
30. Kedia, G.; Vázquez, J.A.; Pandiella, S.S. Evaluation of the fermentability of oat fractions obtained by debranning using lactic acid bacteria. J. Appl. Microbiol. 2008, 105, 1227-1237.
31. Capozzi, V.; Menga, V.; Digesù, A.M.; de Vita, P.; van Sinderen, D.; Cattivelli, L.; Fares, C.; Spano, G. Biotechnological production of vitamin B2-enriched bread and pasta. J. Agric. Food Chem. 2011, 59, 8013-8020.
32. Russo, P.; Capozzi, V.; Arena, M.P.; Spadaccino, G.; Dueñas, M.T.; López, P.; Fiocco, D.; Spano, G. Riboflavin overproducing strains of Lactobacillus fermentum for riboflavin enriched bread. Appl. Microbiol. Biotechnol. 2014, doi:10.1007/s00253-013-5484-7.
33. Crittenden, R.; Karppinen, S.; Ojanen, S.; Tenkanen, M.; Fagerstr. m, R.; Mtt., J.; Saarela, M.; Mattila-Sandholm, T.; Poutanen, K. In vitro fermentation of cereal dietary fibre carbohydrates by probiotic and intestinal bacteria. J. Sci. Food Agric. 2002, 82, 781-789.
34. Johansson, L.; Tuomainen, P.; Anttila, H.; Rita, H.; Virkki, L. Effect of processing on the extractability of oat β-glucan. Food Chem. 2007, 105, 1439-1445.
35. Tosh, S.M.; Brummer, Y.; Wolever, T.M.S.; Wood, P.J. Glycemic response to oat bran muffins treated to vary molecular weight of β-glucan. Cereal Chem. 2008, 85, 211-217.
36. Åman, P.; Rimsten, L.; Andersson, R. Molecular weight distribution of β-glucan in oat-based foods. Cereal Chem. 2004, 81, 356-360.
37. Russo, P.; López, P.; Capozzi, V.; Fernández de Palencia, P.; Dueñas, M.T.; Spano, G.; Fiocco, D. β-Glucans improve growth, viability and colonization of probiotic microorganisms. Int. J. Mol. Sci. 2012, 13, 6026-6039.
38. Su, P.; Henriksson, A.; Mitchell, H. Selected prebiotics support the growth of probiotic mono-cultures in vitro. Food Microbiol. 2007, 13, 134-139.
39. Bove, P.; Russo, P.; Capozzi, V.; Gallone, A.; Spano, G.; Fiocco, D. Lactobacillus plantarum passage through an oro-gastro-intestinal tract simulator: Carrier matrix effect and transcriptional analysis of genes associated to stress and probiosis. Microbiol. Res. 2013, 168, 351-359.
40. Fernández de Palencia, P.; Werning, M.L.; Sierra-Filardi, E.; Dueñas, M.T.; Irastorza, A.; Corbí, A.L.; López, P. Probiotic properties of the 2-Substituted (1,3)-β-D-glucan-producing bacterium Pediococcus parvulus 2.6. Appl. Environ. Microbiol. 2009, 75, 4887-4891.
41. Both, E.; György, É.; Kibédi-Szabó, C.Z.; Tamás, É.; Ábrahám, B.; Miklóssy, I.; Lányi, S. Acid and bile tolerance, adhesion to epithelial cells of probiotic microorganisms. UPB Sci. Bull. B 2010, 72, 37-44.
42. Bezkorovainy, A. Probiotics: Determinants of survival and growth in the gut. Am. J. Clin. Nutr. 2001, 73, 399S-405S.
43. De Vrese, M.; Schrezenmeir, J. Probiotics, prebiotics, and synbiotics. Food Biotechnol. 2008, 11, 1-66.
44. Morelli, L. In vitro selection of probiotic lactobacilli: A critical appraisal. Curr. Issues Intest. Microbiol. 2000, 1, 59-67.
45. Ouwehand, A.C.; Salminen, S. In vitro adhesion assays for probiotics and their in vivo relevance: A review. Microb. Ecol. Health Dis. 2003, 15, 175-184.
46. Stack, H.M.; Kearney, N.; Stanton, C.; Fitzgerald, G.F.; Ross, R.P. Association of β-glucan endogenous production with increased stress tolerance of intestinal lactobacilli. Appl. Environ. Microbiol. 2010, 76, 500-507.
47. Abu Mweis, S.S.; Jew, S.; Ames, N.P. β-glucan from barley and its lipid-lowering capacity: A meta-analysis of randomized, controlled trials. Eur. J. Clin. Nutr. 2010, 64, 1472-1480.
48. Rieder, A.; Knutsen, S.H.; Ballance, S.; Grimmer, S.; Airado-Rodríguez, D. Cereal β-glucan quantification with calcofluor-application to cell culture supernatants. Carbohydr. Polym. 2012, 90, 1564-1572.
49. Meijerink, M.; Wells, J.M.; Taverne, N.; de Zeeuw Brouwer, M.-L.; Hilhorst, B.; Venema, K.; van Bilsen, J. Immunomodulatory effects of potential probiotics in a mouse peanut sensitization model. FEMS Immunol. Med. Microbiol. 2012, 65, 488-496.
50. Van Hemert, S.; Meijerink, M.; Molenaar, D.; Bron, P.A.; de Vos, P.; Kleerebezem, M.; Well, J.M.; Marco, M. L. Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells. BMC Microbiol. 2010, 10, 293-305.
51. Sheu, B.S.; Wu, J.; Lo, C.Y.; Wu, H.W.; Chen, J.H.; Lin, Y.S.; Lin, M.D. Impact of supplement with lactobacillus and bifidobacterium-containing yoghurt on triple therapy for Helicobacter pylori eradication. Aliment. Pharmacol. Ther. 2002, 16, 1669-1675.
52. Macouzet, M.; Lee, B.H.; Robert, N. Production of conjugated linoleic acid by probiotic Lactobacillus acidophilus La5. J. Appl. Microbiol. 2009, 106, 1886-1891.