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Effects of prebiotics on immune system and cytokine expression

Abstract

Nowadays, use of prebiotics as feed and food additives has received increasing interest because of the beneficial effects of prebiotics on the health of animals and humans. One of the beneficial effects of prebiotics is stimulation of immune system, which can be direct or indirect through increasing population of beneficial microbes or probiotics, especially lactic acid bacteria and bifidobacteria, in the gut. An important mechanism of action of probiotics and prebiotics, by which they can affect the immune system, is changing the expression of cytokines. The present review tried to summarize the findings of studies that investigated the effects of prebiotics on immune system with focusing on their effects on cytokine expression. Generally, most of reviewed studies indicated beneficial effects for prebiotics in terms of improving immune system, by increasing the expression of anti-inflammatory cytokines, while reducing the expressions of proinflammatory cytokines. However, most of studies mainly considered the indirect effects of prebiotics on the immune system (through changing the composition and population of gut microbiota), and their direct effects still need to be further studied using prebiotics with different degree of polymerization in different hosts.

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References

  1. 1.

    Badia R, Brufau MT, Guerrero-Zamora AM, Lizardo R, Dobrescu I, Martin-Venegas R, Ferrer R, Salmon H, Martínez P, Brufau J (2012) β-Galactomannan and Saccharomyces cerevisiae var. Boulardii modulate the immune response against Salmonella enterica serovar Typhimurium in porcine intestinal epithelial and dendritic cells. Clin Vaccine Immunol 19:368–376

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Badia R, Zanello G, Chevaleyre C, Lizardo R, Meurens F, Martínez P, Brufau J, Salmon H (2012) Effect of Saccharomyces cerevisiae var. Boulardii and β-galactomannan oligosaccharide on porcine intestinal epithelial and dendritic cells challenged in vitro with Escherichia coli F4 (K88). Vet Res 43:4–15

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Bandeira A, Mota-Santos T, Itohara S, Degermann S, Heusser C, Tonegawa S, Coutinho A (1990) Localization of gamma/delta T cells to the intestinal epithelium is independent of normal microbial colonization. J Exp Med 172:239–244

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, Muir AI, Wigglesworth MJ, Kinghorn I, Fraser NJ (2003) The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 278:11312–11319

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Cani PD, Possemiers S, Van De Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM (2009) Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58:1091–1103

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Cavaglieri CR, Nishiyama A, Fernandes LC, Curi R, Miles EA, Calder PC (2003) Differential effects of short-chain fatty acids on proliferation and production of pro-and anti-inflammatory cytokines by cultured lymphocytes. Life Sci 73:1683–1690

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Clark RSB, Kochanek P (eds) (2012) Brain injury. Springer Science & Business Media, Berlin

    Google Scholar 

  8. 8.

    Dehghan P, Gargari BP, Jafar-Abadi MA (2014) Oligofructose-enriched inulin improves some inflammatory markers and metabolic endotoxemia in women with type 2 diabetes mellitus: a randomized controlled clinical trial. Nutrition 30:418–423

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Denji KA, Mansour MR, Akrami R, Ghobadi S, Jafarpour S, Mirbeygi S (2015) Effect of dietary prebiotic mannan oligosaccharide (MOS) on growth performance, intestinal microflora, body composition, haematological and blood serum biochemical parameters of rainbow trout (Oncorhynchus mykiss) juveniles. J Fish Aquat Sci 10:255

    Article  Google Scholar 

  10. 10.

    Deshmane SL, Kremlev S, Amini S, Sawaya BE (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29:313–326

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Dinarello CA (2011) Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 117:3720–3732

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Faghfoori Z, Navai L, Shakerhosseini R, Somi MH, Nikniaz Z, Norouzi MF (2011) Effects of an oral supplementation of germinated barley foodstuff on serum tumour necrosis factor-α, interleukin-6 and-8 in patients with ulcerative colitis. Ann Clin Biochem 48:233–237

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Furrie E, Macfarlane S, Kennedy A, Cummings JH, Walsh SV, O’neil DA, Macfarlane GT (2005) Synbiotic therapy (Bifidobacterium longum/Synergy 1) initiates resolution of inflammation in patients with active ulcerative colitis: a randomised controlled pilot trial. Gut 54:242–249

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Gibson GR, Probert HM, Van Loo J, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17:259–275

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Gibson GR, Roberfroid MB (1995) Dietary modulation of the colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412

    CAS  PubMed  Google Scholar 

  16. 16.

    Herfel TM, Jacobi SK, Lin X, Fellner V, Walker DC, Jouni ZE, Odle J (2011) Polydextrose enrichment of infant formula demonstrates prebiotic characteristics by altering intestinal microbiota, organic acid concentrations, and cytokine expression in suckling piglets. J Nutr 141:2139–2145

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Hoentjen F, Tannock G, Mulder C, Dieleman L (2006) The prebiotic combination inulin/oligofructose prevents colitis in HLA-B27 rats by immunomodulation and changes in intestinal microflora. Eur J Gastroenterol Hepatol 18:A27

    Article  Google Scholar 

  18. 18.

    Hoentjen F, Welling GW, Harmsen HJ, Zhang X, Snart J, Tannock GW, Lien K, Churchill TA, Lupicki M, Dieleman LA (2005) Reduction of colitis by prebiotics in HLA-B27 transgenic rats is associated with microflora changes and immunomodulation. Inflamm Bowel Dis 11:977–985

    Article  PubMed  Google Scholar 

  19. 19.

    Hosono A, Ozawa A, Kato R, Ohnishi Y, Nakanishi Y, Kimura T, Nakamura R (2003) Dietary fructooligosaccharides induce immunoregulation of intestinal IgA secretion by murine Peyer’s patch cells. Biosci Biotechnol Biochem 67:758–764

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Huang RL, Deng ZY, Yang CB, Yin YL, Xie MY, Wu GY, Li TJ, Li LL, Tang ZR, Kang P (2007) Dietary oligochitosan supplementation enhances immune status of broilers. J Sci Food Agric 87:153–159

    CAS  Article  Google Scholar 

  21. 21.

    Ito H, Takemura N, Sonoyama K, Kawagishi H, Topping DL, Conlon MA, Morita T (2011) Degree of polymerization of inulin-type fructans differentially affects number of lactic acid bacteria, intestinal immune functions, and immunoglobulin A secretion in the rat cecum. J Agric Food Chem 59:5771–5778

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Jahromi MF, Altaher YW, Shokryazdan P, Ebrahimi R, Ebrahimi M, Idrus Z, Goh YM, Tufarelli V, Liang JB (2015) Dietary supplementation of a mixture of Lactobacillus strains enhances performance of broiler chickens raised under heat stress conditions. Int J Biometeorol. doi:10.1007/s00484-015-1103-x

    Google Scholar 

  23. 23.

    Jahromi MF, Liang JB, Shokryazdan P, Ebrahimi R, Navidshad B, Abdullah N (2015) Extraction and characterization of oligosaccharides from palm kernel cake. Bioresources 11:674–695

    Google Scholar 

  24. 24.

    Khadka A (2014) Interleukins in therapeutics. PharmaTutor 2:67–72

    Google Scholar 

  25. 25.

    Klatt NR, Canary LA, Sun X, Vinton CL, Funderburg NT, Morcock DR, Quiñones M, Deming CB, Perkins M, Hazuda DJ (2013) Probiotic/prebiotic supplementation of antiretrovirals improves gastrointestinal immunity in SIV-infected macaques. J Clin Invest 123:903–907

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Kogut MH, Swaggerty CL (2012) Effects of prebiotics and probiotics on the host immune response. In: Callaway TR, Ricke SC (eds) Direct-fed microbials and prebiotics for animals. Springer, New York

    Google Scholar 

  27. 27.

    Lackie J (2010) A dictionary of biomedicine. Oxford University Press, Oxford

    Google Scholar 

  28. 28.

    Langen LV, Mirjam A, Dieleman LA (2009) Prebiotics in chronic intestinal inflammation. Inflamm Bowel Dis 15:454–462

    Article  Google Scholar 

  29. 29.

    Lecerf J-M, Dépeint F, Clerc E, Dugenet Y, Niamba CN, Rhazi L, Cayzeele A, Abdelnour G, Jaruga A, Younes H (2012) Xylo-oligosaccharide (XOS) in combination with inulin modulates both the intestinal environment and immune status in healthy subjects, while XOS alone only shows prebiotic properties. Br J Nutr 108:1847–1858

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Macdonald TT, Monteleone G (2001) IL-12 and Th1 immune responses in human Peyer’s patches. Trends Immunol 22:244–247

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Martin R, Nauta A, Ben Amor K, Knippels L, Knol J, Garssen J (2010) Early life: gut microbiota and immune development in infancy. Benef Microbes 1:367–382

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Mccarville J (2012) Effects of prebiotic fibre diets on rat mucosal intestinal and systemic immunity and in vitro mechanistic analysis of anti-inflammatory effects of Lactobacillus strains on rat and human intestinal epithelial cells. http://hdl.handle.net/10155/275

  33. 33.

    Medzhitov R (2007) Recognition of microorganisms and activation of the immune response. Nature 449:819–826

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    Murarolli VDA, Burbarelli MFC, Polycarpo GV, Ribeiro PAP, Moro MEG, Albuquerque R (2014) Prebiotic, probiotic and symbiotic as alternative to antibiotics on the performance and Immune response of broiler chickens. Rev Bras Cienc Avic 16:279–284

    Article  Google Scholar 

  35. 35.

    Nagura T, Hachimura S, Hashiguchi M, Ueda Y, Kanno T, Kikuchi H, Sayama K, Kaminogawa S (2002) Suppressive effect of dietary raffinose on T-helper 2 cell-mediated immunity. Br J Nutr 88:421–426

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Olivier JG, Van Aardenne JA, Dentener FJ, Pagliari V, Ganzeveld LN, Peters JA (2005) Recent trends in global greenhouse gas emissions: regional trends 1970–2000 and spatial distribution of key sources in 2000. Environ Sci 2:81–99

    Article  Google Scholar 

  37. 37.

    Oyofo BA, Deloach JR, Corrier DE, Norman JO, Ziprin RL, Mollenhauer HH (1989) Prevention of Salmonella typhimurium colonization of broilers with d-mannose. Poult Sci 68:1357–1360

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118:229–241

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Rodríguez-Cabezas ME, Camuesco D, Arribas B, Garrido-Mesa N, Comalada M, Bailón E, Cueto-Sola M, Utrilla P, Guerra-Hernández E, Pérez-Roca C (2010) The combination of fructooligosaccharides and resistant starch shows prebiotic additive effects in rats. Clin Nutr 29:832–839

    Article  PubMed  Google Scholar 

  40. 40.

    Roller M, Rechkemmer G, Watzl B (2004) Prebiotic inulin enriched with oligofructose in combination with the probiotics Lactobacillus rhamnosus and Bifidobacterium lactis modulates intestinal immune functions in rats. J Nutr 134:153–156

    CAS  PubMed  Google Scholar 

  41. 41.

    Seifert S, Watzl B (2007) Inulin and oligofructose: review of experimental data on immune modulation. J Nutr 137:2563–2567

    Google Scholar 

  42. 42.

    Shokryazdan P, Sieo CC, Kalavathy R, Liang JB, Alitheen NB, Faseleh Jahromi M, Ho YW (2014) Probiotic potential of Lactobacillus strains with antimicrobial activity against some human pathogenic strains. Biomed Res Int. doi:10.1155/2014/927268

    PubMed  PubMed Central  Google Scholar 

  43. 43.

    Sims JE, March CJ, Cosman D, Widmer MB, Macdonald HR, Mcmahan CJ, Grubin CE, Wignall JM, Jackson JL, Call SM (1988) cDNA expression cloning of the IL-1 receptor, a member of the immunoglobulin superfamily. Science 241:585–589

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Steed H, Macfarlane S (2009) Mechanisms of prebiotic impact on health. In: Charalampopoulos D, Rastall RA (eds) Prebiotics and probiotics science and technology. Springer Science & Business Media, Berlin

    Google Scholar 

  45. 45.

    Takahashí T, Nakagawa E, Nara T, Yajima T, Kuwata T (1998) Effects of orally ingested Bifidobacterium longum on the mucosal IgA response of mice to dietary antigens. Biosci Biotechnol Biochem 62:10–15

    Article  PubMed  Google Scholar 

  46. 46.

    Vance RE, Isberg RR, Portnoy DA (2009) Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6:10–21

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR (2008) Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. Am J Clin Nutr 88:1438–1446

    CAS  PubMed  Google Scholar 

  48. 48.

    Wilson KH, Blitchington RB (1996) Human colonic biota studied by ribosomal DNA sequence analysis. Appl Environ Microbiol 62:2273–2278

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Younger P (2007) Stedman’s medical dictionary. Ref Rev 21:41–42

    Google Scholar 

  50. 50.

    Zhang J-M, An J (2007) Cytokines, inflammation and pain. Int Anesthesiol Clin 45:27–37

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The present study was supported by the Ministry of Higher Education Malaysia under the LRGS Fasa 1/2012 grant, UPM/700-1/3/LRGS.

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Correspondence to Juan Boo Liang.

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Shokryazdan, P., Faseleh Jahromi, M., Navidshad, B. et al. Effects of prebiotics on immune system and cytokine expression. Med Microbiol Immunol 206, 1–9 (2017). https://doi.org/10.1007/s00430-016-0481-y

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Keywords

  • Prebiotic
  • Oligosaccharide
  • Cytokine
  • Immunomodulatory
  • Inflammatory