Skip to main content

Advertisement

Log in

Engineering the Microbiome: a Novel Approach to Immunotherapy for Allergic and Immune Diseases

  • Immunotherapy and Immunomodulators (B Vickery, Section Editor)
  • Published:
Current Allergy and Asthma Reports Aims and scope Submit manuscript

Abstract

The incidence of immune disorders is growing parallel with practices associated with westernization, such as dietary changes, increased use of antibiotics, or elevated rates of Cesarean section. These practices can significantly impact the gut microbiota, the collection of bacteria residing in the human gastrointestinal tract, and subsequently disrupt the delicate balance existing between commensal flora and host immune responses. Restoring this balance by modifying the microbiota has thus emerged as a promising therapeutic approach. Here, we discuss the interaction between gut commensals and immunity, along with the potential of different interventions on the microbiota as treatment for inflammatory and allergic diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Sicherer SH, Munoz-Furlong A, Godbold JH, Sampson HA. US prevalence of self-reported peanut, tree nut, and sesame allergy: 11-year follow-up. J Allergy Clin Immunol. 2010;125:1322–6. doi:10.1016/j.jaci.2010.03.029.

    CAS  PubMed  Google Scholar 

  2. Molodecky NA et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 2012;142:46–54. doi:10.1053/j.gastro.2011.10.001. e42; quiz e30.

    PubMed  Google Scholar 

  3. Grundy J, Matthews S, Bateman B, Dean T, Arshad SH. Rising prevalence of allergy to peanut in children: data from 2 sequential cohorts. J Allergy Clin Immunol. 2002;110:784–9.

    PubMed  Google Scholar 

  4. Mullins RJ, Dear KB, Tang ML. Characteristics of childhood peanut allergy in the Australian Capital Territory, 1995 to 2007. J Allergy Clin Immunol. 2009;123:689–93. doi:10.1016/j.jaci.2008.12.1116.

    PubMed  Google Scholar 

  5. Eder W, Ege MJ, von Mutius E. The asthma epidemic. N Engl J Med. 2006;355:2226–35. doi:10.1056/NEJMra054308.

    CAS  PubMed  Google Scholar 

  6. Dominguez-Bello MG et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci U S A. 2010;107:11971–5. doi:10.1073/pnas.1002601107.

    PubMed Central  PubMed  Google Scholar 

  7. Cox LM et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014;158:705–21. doi:10.1016/j.cell.2014.05.052.

    CAS  PubMed  Google Scholar 

  8. Thorburn AN, Macia L, Mackay CR. Diet, metabolites, and “western-lifestyle” inflammatory diseases. Immunity. 2014;40:833–42. doi:10.1016/j.immuni.2014.05.014.

    CAS  PubMed  Google Scholar 

  9. Garrett WS et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell. 2007;131:33–45. doi:10.1016/j.cell.2007.08.017.

    CAS  PubMed Central  PubMed  Google Scholar 

  10. Noval Rivas M et al. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J Allergy Clin Immunol. 2013;131:201–12. doi:10.1016/j.jaci.2012.10.026. This article demonstrates the existence of transmissible allergy-prone microbiota, linking gut microbiota to food allergy directly for the first time.

    CAS  PubMed  Google Scholar 

  11. Trompette A et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med. 2014;20:159–66. doi:10.1038/nm.3444. This study shows evidence at the cellular level of an association between gut microbiota and bone marrow hemapoiesis, suggesting the microbiota can be a target for immune disorders at some sites other than in the GI tract.

    CAS  PubMed  Google Scholar 

  12. Rajilic-Stojanovic M, Heilig HG, Tims S, Zoetendal EG, de Vos WM. Long-term monitoring of the human intestinal microbiota composition. Environ Microbiol. 2012. doi:10.1111/1462-2920.12023.

    PubMed  Google Scholar 

  13. Faith JJ et al. The long-term stability of the human gut microbiota. Science. 2013;341:1237439. doi:10.1126/science.1237439.

    PubMed Central  PubMed  Google Scholar 

  14. Koropatkin NM, Cameron EA, Martens EC. How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol. 2012;10:323–35. doi:10.1038/nrmicro2746.

    CAS  PubMed Central  PubMed  Google Scholar 

  15. Bird JJ et al. Helper T cell differentiation is controlled by the cell cycle. Immunity. 1998;9:229–37.

    CAS  PubMed  Google Scholar 

  16. Peng L, He Z, Chen W, Holzman IR, Lin J. Effects of butyrate on intestinal barrier function in a Caco-2 cell monolayer model of intestinal barrier. Pediatr Res. 2007;61:37–41. doi:10.1203/01.pdr.0000250014.92242.f3.

    CAS  PubMed  Google Scholar 

  17. Yatsunenko T et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–7. doi:10.1038/nature11053.

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Martin R et al. Early life: gut microbiota and immune development in infancy. Benefic Microbes. 2010;1:367–82. doi:10.3920/BM2010.0027.

    CAS  Google Scholar 

  19. Ouwehand AC. Antiallergic effects of probiotics. J Nutr. 2007;137:794S–7.

    CAS  PubMed  Google Scholar 

  20. Debock I, Flamand V. Unbalanced neonatal CD4(+) T-cell immunity. Front Immunol. 2014;5:393. doi:10.3389/fimmu.2014.00393.

    PubMed Central  PubMed  Google Scholar 

  21. von der Weid T, Bulliard C, Schiffrin EJ. Induction by a lactic acid bacterium of a population of CD4(+) T cells with low proliferative capacity that produce transforming growth factor beta and interleukin-10. Clin Diagn Lab Immunol. 2001;8:695–701. doi:10.1128/CDLI.8.4.695-701.2001.

    PubMed Central  PubMed  Google Scholar 

  22. Kirjavainen PV, Gibson GR. Healthy gut microflora and allergy: factors influencing development of the microbiota. Ann Med. 1999;31:288–92.

    CAS  PubMed  Google Scholar 

  23. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol. 2008;8:411–20. doi:10.1038/nri2316.

    CAS  PubMed  Google Scholar 

  24. Kim HG et al. Lactobacillus plantarum lipoteichoic acid down-regulated Shigella flexneri peptidoglycan-induced inflammation. Mol Immunol. 2011;48:382–91. doi:10.1016/j.molimm.2010.07.011.

    CAS  PubMed  Google Scholar 

  25. Fukuda S, Toh H, Taylor TD, Ohno H, Hattori M. Acetate-producing bifidobacteria protect the host from enteropathogenic infection via carbohydrate transporters. Gut Microbes. 2012;3:449–54. doi:10.4161/gmic.21214.

    PubMed  Google Scholar 

  26. Esplugues E et al. Control of TH17 cells occurs in the small intestine. Nature. 2011;475:514–8. doi:10.1038/nature10228.

    CAS  PubMed Central  PubMed  Google Scholar 

  27. Ivanov II et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139:485–98. doi:10.1016/j.cell.2009.09.033.

    CAS  PubMed Central  PubMed  Google Scholar 

  28. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005;122:107–18. doi:10.1016/j.cell.2005.05.007.

    CAS  PubMed  Google Scholar 

  29. Round JL et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science. 2011;332:974–7. doi:10.1126/science.1206095.

    CAS  PubMed Central  PubMed  Google Scholar 

  30. Atarashi K et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011;331:337–41. doi:10.1126/science.1198469.

    CAS  PubMed Central  PubMed  Google Scholar 

  31. Sokol H et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008;105:16731–6. doi:10.1073/pnas.0804812105.

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Wang J. Food allergy: recent advances in pathophysiology and treatment. Allergy Asthma Immunol Res. 2009;1:19–29. doi:10.4168/aair.2009.1.1.19.

    PubMed Central  PubMed  Google Scholar 

  33. Kunisawa J, Kiyono H. Aberrant interaction of the gut immune system with environmental factors in the development of food allergies. Curr Allergy Asthma Rep. 2010;10:215–21. doi:10.1007/s11882-010-0097-z.

    PubMed  Google Scholar 

  34. Berin MC, Mayer L. Can we produce true tolerance in patients with food allergy? J Allergy Clin Immunol. 2013;131:14–22. doi:10.1016/j.jaci.2012.10.058.

    CAS  PubMed  Google Scholar 

  35. Noverr MC, Huffnagle GB. The ‘microflora hypothesis’ of allergic diseases. Clin Exp Allergy : J Br Soc Allergy Clin Immunol. 2005;35:1511–20. doi:10.1111/j.1365-2222.2005.02379.x.

    CAS  Google Scholar 

  36. Penders J, Stobberingh EE, van den Brandt PA, Thijs C. The role of the intestinal microbiota in the development of atopic disorders. Allergy. 2007;62:1223–36. doi:10.1111/j.1398-9995.2007.01462.x.

    CAS  PubMed  Google Scholar 

  37. Viljanen M et al. Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy. 2005;60:494–500. doi:10.1111/j.1398-9995.2004.00514.x.

    CAS  PubMed  Google Scholar 

  38. Pohjavuori E et al. Lactobacillus GG effect in increasing IFN-gamma production in infants with cow’s milk allergy. J Allergy Clin Immunol. 2004;114:131–6. doi:10.1016/j.jaci.2004.03.036.

    CAS  PubMed  Google Scholar 

  39. Sanchez E, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. Intestinal Bacteroides species associated with coeliac disease. J Clin Pathol. 2010;63:1105–11. doi:10.1136/jcp.2010.076950.

    CAS  PubMed  Google Scholar 

  40. Collado MC, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. Specific duodenal and faecal bacterial groups associated with paediatric coeliac disease. J Clin Pathol. 2009;62:264–9. doi:10.1136/jcp.2008.061366.

    CAS  PubMed  Google Scholar 

  41. Collado MC, Donat E, Ribes-Koninckx C, Calabuig M, Sanz Y. Imbalances in faecal and duodenal Bifidobacterium species composition in active and non-active coeliac disease. BMC Microbiol. 2008;8:232. doi:10.1186/1471-2180-8-232.

    PubMed Central  PubMed  Google Scholar 

  42. Sartor RB. Mechanisms of disease: pathogenesis of Crohn’s disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol. 2006;3:390–407. doi:10.1038/ncpgasthep0528.

    CAS  PubMed  Google Scholar 

  43. Spehlmann ME et al. Epidemiology of inflammatory bowel disease in a German twin cohort: results of a nationwide study. Inflamm Bowel Dis. 2008;14:968–76. doi:10.1002/ibd.20380.

    PubMed  Google Scholar 

  44. Orholm M, Binder V, Sorensen TI, Rasmussen LP, Kyvik KO. Concordance of inflammatory bowel disease among Danish twins. Results of a nationwide study. Scand J Gastroenterol. 2000;35:1075–81.

    CAS  PubMed  Google Scholar 

  45. Halfvarson J, Bodin L, Tysk C, Lindberg E, Jarnerot G. Inflammatory bowel disease in a Swedish twin cohort: a long-term follow-up of concordance and clinical characteristics. Gastroenterology. 2003;124:1767–73.

    PubMed  Google Scholar 

  46. Prescott NJ et al. A nonsynonymous SNP in ATG16L1 predisposes to ileal Crohn’s disease and is independent of CARD15 and IBD5. Gastroenterology. 2007;132:1665–71. doi:10.1053/j.gastro.2007.03.034.

    CAS  PubMed  Google Scholar 

  47. Sartor RB. Current concepts of the etiology and pathogenesis of ulcerative colitis and Crohn’s disease. Gastroenterol Clin N Am. 1995;24:475–507.

    CAS  Google Scholar 

  48. Sellon RK et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun. 1998;66:5224–31.

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Kullberg MC et al. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect Immun. 1998;66:5157–66.

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Devkota S et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature. 2012;487:104–8. doi:10.1038/nature11225.

    CAS  PubMed Central  PubMed  Google Scholar 

  51. Balish E, Warner T. Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am J Pathol. 2002;160:2253–7. doi:10.1016/S0002-9440(10)61172-8.

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Kim SC et al. Variable phenotypes of enterocolitis in interleukin 10-deficient mice monoassociated with two different commensal bacteria. Gastroenterology. 2005;128:891–906.

    CAS  PubMed  Google Scholar 

  53. Machiels K et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. 2014;63:1275–83. doi:10.1136/gutjnl-2013-304833.

    CAS  PubMed  Google Scholar 

  54. Gevers D et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe. 2014;15:382–92. doi:10.1016/j.chom.2014.02.005.

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Tong M et al. A modular organization of the human intestinal mucosal microbiota and its association with inflammatory bowel disease. PLoS One. 2013;8, e80702. doi:10.1371/journal.pone.0080702.

    PubMed Central  PubMed  Google Scholar 

  56. Morgan XC et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13:R79. doi:10.1186/gb-2012-13-9-r79.

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Turroni F et al. Diversity of bifidobacteria within the infant gut microbiota. PLoS One. 2012;7, e36957. doi:10.1371/journal.pone.0036957.

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Le Pendu J. Histo-blood group antigen and human milk oligosaccharides: genetic polymorphism and risk of infectious diseases. Adv Exp Med Biol. 2004;554:135–43.

    PubMed  Google Scholar 

  59. Verhasselt V. Neonatal tolerance under breastfeeding influence. Curr Opin Immunol. 2010;22:623–30. doi:10.1016/j.coi.2010.08.008.

    CAS  PubMed  Google Scholar 

  60. Labeta MO et al. Innate recognition of bacteria in human milk is mediated by a milk-derived highly expressed pattern recognition receptor, soluble CD14. J Exp Med. 2000;191:1807–12.

    CAS  PubMed Central  PubMed  Google Scholar 

  61. LeBouder E et al. Soluble forms of Toll-like receptor (TLR)2 capable of modulating TLR2 signaling are present in human plasma and breast milk. J Immunol. 2003;171:6680–9.

    CAS  PubMed  Google Scholar 

  62. Martin R et al. Cultivation-independent assessment of the bacterial diversity of breast milk among healthy women. Res Microbiol. 2007;158:31–7. doi:10.1016/j.resmic.2006.11.004.

    PubMed  Google Scholar 

  63. Adlerberth I, Wold AE. Establishment of the gut microbiota in Western infants. Acta Paediatr. 2009;98:229–38. doi:10.1111/j.1651-2227.2008.01060.x.

    CAS  PubMed  Google Scholar 

  64. Jalanka-Tuovinen J et al. Intestinal microbiota in healthy adults: temporal analysis reveals individual and common core and relation to intestinal symptoms. PLoS One. 2011;6, e23035. doi:10.1371/journal.pone.0023035.

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Hehemann JH et al. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature. 2010;464:908–12. doi:10.1038/nature08937.

    CAS  PubMed  Google Scholar 

  66. Wu GD et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334:105–8. doi:10.1126/science.1208344.

    CAS  PubMed Central  PubMed  Google Scholar 

  67. Begley M, Gahan CG, Hill C. The interaction between bacteria and bile. FEMS Microbiol Rev. 2005;29:625–51. doi:10.1016/j.femsre.2004.09.003.

    CAS  PubMed  Google Scholar 

  68. Jantchou P, Morois S, Clavel-Chapelon F, Boutron-Ruault MC, Carbonnel F. Animal protein intake and risk of inflammatory bowel disease: the E3N prospective study. Am J Gastroenterol. 2010;105:2195–201. doi:10.1038/ajg.2010.192.

    CAS  PubMed  Google Scholar 

  69. Walker AW et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5:220–30. doi:10.1038/ismej.2010.118.

    CAS  PubMed Central  PubMed  Google Scholar 

  70. Fallingborg J. Intraluminal pH of the human gastrointestinal tract. Dan Med Bull. 1999;46:183–96.

    CAS  PubMed  Google Scholar 

  71. Duncan SH, Louis P, Thomson JM, Flint HJ. The role of pH in determining the species composition of the human colonic microbiota. Environ Microbiol. 2009;11:2112–22. doi:10.1111/j.1462-2920.2009.01931.x.

    PubMed  Google Scholar 

  72. Zimmer J et al. A vegan or vegetarian diet substantially alters the human colonic faecal microbiota. Eur J Clin Nutr. 2012;66:53–60. doi:10.1038/ejcn.2011.141.

    CAS  PubMed  Google Scholar 

  73. Watson D et al. Selective carbohydrate utilization by lactobacilli and bifidobacteria. J Appl Microbiol. 2013;114:1132–46. doi:10.1111/jam.12105.

    CAS  PubMed  Google Scholar 

  74. Furusawa Y et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504:446–50. doi:10.1038/nature12721.

    CAS  PubMed  Google Scholar 

  75. Fukuda S et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011;469:543–7. doi:10.1038/nature09646.

    CAS  PubMed  Google Scholar 

  76. Maslowski KM et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461:1282–6. doi:10.1038/nature08530.

    CAS  PubMed Central  PubMed  Google Scholar 

  77. Palmer DJ, Makrides M. Diet of lactating women and allergic reactions in their infants. Curr Opin Clin Nutr Metab Care. 2006;9:284–8. doi:10.1097/01.mco.0000222113.46042.50.

    CAS  PubMed  Google Scholar 

  78. Verhasselt V et al. Breast milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma. Nat Med. 2008;14:170–5. doi:10.1038/nm1718.

    CAS  PubMed  Google Scholar 

  79. Coombes JL et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med. 2007;204:1757–64. doi:10.1084/jem.20070590.

    CAS  PubMed Central  PubMed  Google Scholar 

  80. Mora JR et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science. 2006;314:1157–60. doi:10.1126/science.1132742.

    CAS  PubMed  Google Scholar 

  81. Mucida D et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science. 2007;317:256–60. doi:10.1126/science.1145697.

    CAS  PubMed  Google Scholar 

  82. Iwata M et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity. 2004;21:527–38. doi:10.1016/j.immuni.2004.08.011.

    CAS  PubMed  Google Scholar 

  83. Chang JH, Cha HR, Lee DS, Seo KY, Kweon MN. 1,25-Dihydroxyvitamin D3 inhibits the differentiation and migration of T(H)17 cells to protect against experimental autoimmune encephalomyelitis. PLoS One. 2010;5, e12925. doi:10.1371/journal.pone.0012925.

    PubMed Central  PubMed  Google Scholar 

  84. Bruce D, Cantorna MT. Intrinsic requirement for the vitamin D receptor in the development of CD8alphaalpha-expressing T cells. J Immunol. 2011;186:2819–25. doi:10.4049/jimmunol.1003444.

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Sonnenberg GF, Fouser LA, Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol. 2011;12:383–90. doi:10.1038/ni.2025.

    CAS  PubMed  Google Scholar 

  86. Li Y et al. Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation. Cell. 2011;147:629–40. doi:10.1016/j.cell.2011.09.025.

    CAS  PubMed  Google Scholar 

  87. Kiss EA et al. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science. 2011;334:1561–5. doi:10.1126/science.1214914.

    CAS  PubMed  Google Scholar 

  88. Schulz VJ et al. Activation of the aryl hydrocarbon receptor suppresses sensitization in a mouse peanut allergy model. Toxicol Sci : Off J Soc Toxicol. 2011;123:491–500. doi:10.1093/toxsci/kfr175.

    CAS  Google Scholar 

  89. Wright JD, Wang CY. Trends in intake of energy and macronutrients in adults from 1999-2000 through 2007–2008. NCHS Data Brief 2010; 1–8.

  90. Clemente JC, et al. The microbiome of uncontacted Amerindians. Sci Adv. 2015.

  91. Muegge BD et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332:970–4. doi:10.1126/science.1198719.

    CAS  PubMed Central  PubMed  Google Scholar 

  92. De Filippo C et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107:14691–6. doi:10.1073/pnas.1005963107.

    PubMed Central  PubMed  Google Scholar 

  93. de La Serre CB et al. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol. 2010;299:G440–8. doi:10.1152/ajpgi.00098.2010.

    Google Scholar 

  94. Jowett SL et al. Influence of dietary factors on the clinical course of ulcerative colitis: a prospective cohort study. Gut. 2004;53:1479–84. doi:10.1136/gut.2003.024828.

    CAS  PubMed Central  PubMed  Google Scholar 

  95. Cohen SA et al. Clinical and mucosal improvement with specific carbohydrate diet in pediatric Crohn disease. J Pediatr Gastroenterol Nutr. 2014;59:516–21. doi:10.1097/MPG.0000000000000449.

    CAS  PubMed  Google Scholar 

  96. Suskind DL, Wahbeh G, Gregory N, Vendettuoli H, Christie D. Nutritional therapy in pediatric Crohn disease: the specific carbohydrate diet. J Pediatr Gastroenterol Nutr. 2014;58:87–91. doi:10.1097/MPG.0000000000000103.

    CAS  PubMed  Google Scholar 

  97. Day AS et al. Exclusive enteral feeding as primary therapy for Crohn’s disease in Australian children and adolescents: a feasible and effective approach. J Gastroenterol Hepatol. 2006;21:1609–14. doi:10.1111/j.1440-1746.2006.04294.x.

    PubMed  Google Scholar 

  98. Day AS, Burgess L. Exclusive enteral nutrition and induction of remission of active Crohn’s disease in children. Expert Rev Clin Immunol. 2013;9:375–83. doi:10.1586/eci.13.12. quiz 384.

    CAS  PubMed  Google Scholar 

  99. Wall CL, Day AS, Gearry RB. Use of exclusive enteral nutrition in adults with Crohn’s disease: a review. World J Gastroenterol: WJG. 2013;19:7652–60. doi:10.3748/wjg.v19.i43.7652.

    PubMed Central  PubMed  Google Scholar 

  100. Heuschkel RB, Menache CC, Megerian JT, Baird AE. Enteral nutrition and corticosteroids in the treatment of acute Crohn’s disease in children. J Pediatr Gastroenterol Nutr. 2000;31:8–15.

    CAS  PubMed  Google Scholar 

  101. Tjellstrom B et al. Effect of exclusive enteral nutrition on gut microflora function in children with Crohn’s disease. Scand J Gastroenterol. 2012;47:1454–9. doi:10.3109/00365521.2012.703234.

    PubMed  Google Scholar 

  102. Gerasimidis K et al. Decline in presumptively protective gut bacterial species and metabolites are paradoxically associated with disease improvement in pediatric Crohn’s disease during enteral nutrition. Inflamm Bowel Dis. 2014;20:861–71. doi:10.1097/MIB.0000000000000023.

    PubMed  Google Scholar 

  103. Luna-Pech JA, Torres-Mendoza BM, Garcia-Cobas CY, Navarrete-Navarro S, Elizalde-Lozano AM. Normocaloric diet improves asthma-related quality of life in obese pubertal adolescents. Int Arch Allergy Immunol. 2014;163:252–8. doi:10.1159/000360398.

    PubMed  Google Scholar 

  104. Kim HJ, Yu BP, Chung HY. Molecular exploration of age-related NF-kappaB/IKK downregulation by calorie restriction in rat kidney. Free Radic Biol Med. 2002;32:991–1005.

    CAS  PubMed  Google Scholar 

  105. van den Elsen LW et al. CD25+ regulatory T cells transfer n-3 long chain polyunsaturated fatty acids-induced tolerance in mice allergic to cow’s milk protein. Allergy. 2013;68:1562–70. doi:10.1111/all.12300.

    PubMed  Google Scholar 

  106. van den Elsen LW et al. Dietary long chain n-3 polyunsaturated fatty acids prevent allergic sensitization to cow’s milk protein in mice. Clin Exp Allergy : J Br Soc Allergy Clin Immunol. 2013;43:798–810. doi:10.1111/cea.12111.

    Google Scholar 

  107. van den Elsen LW et al. DHA-rich tuna oil effectively suppresses allergic symptoms in mice allergic to whey or peanut. J Nutr. 2014;144:1970–6. doi:10.3945/jn.114.198515.

    PubMed  Google Scholar 

  108. Ghosh S et al. Fish oil attenuates omega-6 polyunsaturated fatty acid-induced dysbiosis and infectious colitis but impairs LPS dephosphorylation activity causing sepsis. PLoS One. 2013;8, e55468. doi:10.1371/journal.pone.0055468.

    CAS  PubMed Central  PubMed  Google Scholar 

  109. Yang N, Song Y, Sampson H, Li X. Bioactivities of berberine, palmatine, and jatrorrhizine isolated from Food Allergy Herbal Formula 2 (FAHF-2). J Allergy Clin Immunol. 2011;127:AB240. doi:10.1016/j.jaci.2010.12.956.

    Google Scholar 

  110. Zhang X et al. Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats. PLoS One. 2012;7, e42529. doi:10.1371/journal.pone.0042529.

    CAS  PubMed Central  PubMed  Google Scholar 

  111. Wang J. Treatment of food anaphylaxis with traditional Chinese herbal remedies: from mouse model to human clinical trials. Curr Opin Allergy Clin Immunol. 2013;13:386–91. doi:10.1097/ACI.0b013e3283615bc4.

    PubMed Central  PubMed  Google Scholar 

  112. David LA et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–63. doi:10.1038/nature12820.

    CAS  PubMed Central  PubMed  Google Scholar 

  113. Berg D, Clemente JC, Colombel JF. Can inflammatory bowel disease be permanently treated with short-term interventions on the microbiome?. Expert Rev Gastroenterol Hepatol. 2015; 1–15, doi:10.1586/17474124.2015.1013031.

  114. Modi SR, Collins JJ, Relman DA. Antibiotics and the gut microbiota. J Clin Invest. 2014;124:4212–8. doi:10.1172/JCI72333.

    CAS  PubMed  Google Scholar 

  115. Colombel JF et al. A controlled trial comparing ciprofloxacin with mesalazine for the treatment of active Crohn’s disease. Groupe d’Etudes Therapeutiques des Affections Inflammatoires Digestives (GETAID). Am J Gastroenterol. 1999;94:674–8. doi:10.1111/j.1572-0241.1999.935_q.x.

    CAS  PubMed  Google Scholar 

  116. Selby W et al. Two-year combination antibiotic therapy with clarithromycin, rifabutin, and clofazimine for Crohn’s disease. Gastroenterology. 2007;132:2313–9. doi:10.1053/j.gastro.2007.03.031.

    CAS  PubMed  Google Scholar 

  117. Prantera C et al. Rifaximin-extended intestinal release induces remission in patients with moderately active Crohn’s disease. Gastroenterology. 2012;142:473–81. doi:10.1053/j.gastro.2011.11.032. e474.

    CAS  PubMed  Google Scholar 

  118. Leiper K et al. Clinical trial: randomized study of clarithromycin versus placebo in active Crohn’s disease. Aliment Pharmacol Ther. 2008;27:1233–9. doi:10.1111/j.1365-2036.2008.03661.x.

    CAS  PubMed  Google Scholar 

  119. Afdhal NH, Long A, Lennon J, Crowe J, O’Donoghue DP. Controlled trial of antimycobacterial therapy in Crohn’s disease. Clofazimine versus placebo. Dig Dis Sci. 1991;36:449–53.

    CAS  PubMed  Google Scholar 

  120. Sutherland L et al. Double blind, placebo controlled trial of metronidazole in Crohn’s disease. Gut. 1991;32:1071–5.

    CAS  PubMed Central  PubMed  Google Scholar 

  121. Steinhart AH et al. Combined budesonide and antibiotic therapy for active Crohn’s disease: a randomized controlled trial. Gastroenterology. 2002;123:33–40.

    CAS  PubMed  Google Scholar 

  122. Ohkusa T et al. Newly developed antibiotic combination therapy for ulcerative colitis: a double-blind placebo-controlled multicenter trial. Am J Gastroenterol. 2010;105:1820–9. doi:10.1038/ajg.2010.84.

    CAS  PubMed  Google Scholar 

  123. Turunen UM et al. Long-term treatment of ulcerative colitis with ciprofloxacin: a prospective, double-blind, placebo-controlled study. Gastroenterology. 1998;115:1072–8.

    CAS  PubMed  Google Scholar 

  124. Mantzaris GJ et al. A prospective randomized controlled trial of intravenous ciprofloxacin as an adjunct to corticosteroids in acute, severe ulcerative colitis. Scand J Gastroenterol. 2001;36:971–4.

    CAS  PubMed  Google Scholar 

  125. Mantzaris GJ et al. A prospective randomized controlled trial of oral ciprofloxacin in acute ulcerative colitis. Am J Gastroenterol. 1997;92:454–6.

    CAS  PubMed  Google Scholar 

  126. Dickinson RJ et al. Double blind controlled trial of oral vancomycin as adjunctive treatment in acute exacerbations of idiopathic colitis. Gut. 1985;26:1380–4.

    CAS  PubMed Central  PubMed  Google Scholar 

  127. Mantzaris GJ, Hatzis A, Kontogiannis P, Triadaphyllou G. Intravenous tobramycin and metronidazole as an adjunct to corticosteroids in acute, severe ulcerative colitis. Am J Gastroenterol. 1994;89:43–6.

    CAS  PubMed  Google Scholar 

  128. Gionchetti P et al. Antibiotic combination therapy in patients with chronic, treatment-resistant pouchitis. Aliment Pharmacol Ther. 1999;13:713–8.

    CAS  PubMed  Google Scholar 

  129. Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008;6, e280. doi:10.1371/journal.pbio.0060280.

    PubMed Central  PubMed  Google Scholar 

  130. Mattila E et al. Fecal transplantation, through colonoscopy, is effective therapy for recurrent Clostridium difficile infection. Gastroenterology. 2012;142:490–6. doi:10.1053/j.gastro.2011.11.037.

    PubMed  Google Scholar 

  131. van Nood E et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368:407–15. doi:10.1056/NEJMoa1205037.

    PubMed  Google Scholar 

  132. Gough E, Shaikh H, Manges AR. Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection. Clin Infect Dis : Off Publ Infect Dis Soc Am. 2011;53:994–1002. doi:10.1093/cid/cir632.

    Google Scholar 

  133. Youngster I et al. Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA. 2014;312:1772–8. doi:10.1001/jama.2014.13875. This study shows a novel form of FMT using encapsulated frozen microbiota, opening the way for safer and more efficient ways to modulate microbiome content.

    CAS  PubMed  Google Scholar 

  134. Damman CJ, Miller SI, Surawicz CM, Zisman TL. The microbiome and inflammatory bowel disease: is there a therapeutic role for fecal microbiota transplantation? Am J Gastroenterol. 2012;107:1452–9. doi:10.1038/ajg.2012.93.

    PubMed  Google Scholar 

  135. Ianiro G, Bibbo S, Scaldaferri F, Gasbarrini A, Cammarota G. Fecal microbiota transplantation in inflammatory bowel disease: beyond the excitement. Medicine. 2014;93:e97. doi:10.1097/MD.0000000000000097.

    PubMed  Google Scholar 

  136. Shankar V et al. Species and genus level resolution analysis of gut microbiota in Clostridium difficile patients following fecal microbiota transplantation. Microbiome. 2014;2:13. doi:10.1186/2049-2618-2-13.

    PubMed Central  PubMed  Google Scholar 

  137. Smits LP, Bouter KE, de Vos WM, Borody TJ, Nieuwdorp M. Therapeutic potential of fecal microbiota transplantation. Gastroenterology. 2013;145:946–53. doi:10.1053/j.gastro.2013.08.058.

    PubMed  Google Scholar 

Download references

Acknowledgments

JCC was partially supported by funding from SUCCESS.

Compliance with Ethics Guidelines

Conflict of Interest

Nan Shen and Jose C. Clemente declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jose C. Clemente.

Additional information

This article is part of the Topical Collection on Immunotherapy and Immunomodulators

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shen, N., Clemente, J.C. Engineering the Microbiome: a Novel Approach to Immunotherapy for Allergic and Immune Diseases. Curr Allergy Asthma Rep 15, 39 (2015). https://doi.org/10.1007/s11882-015-0538-9

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s11882-015-0538-9

Keywords

Navigation