DOI QR코드

DOI QR Code

Immune Disorders and Its Correlation with Gut Microbiome

  • Hwang, Ji-Sun (School of Life Sciences and Immune Synapse Research Center, Gwangju Institute of Science and Technology (GIST)) ;
  • Im, Chang-Rok (Global Leader Program, Bugil Academy) ;
  • Im, Sin-Hyeog (School of Life Sciences and Immune Synapse Research Center, Gwangju Institute of Science and Technology (GIST))
  • Received : 2012.07.07
  • Accepted : 2012.07.27
  • Published : 2012.08.30

Abstract

Allergic disorders such as atopic dermatitis and asthma are common hyper-immune disorders in industrialized countries. Along with genetic association, environmental factors and gut microbiota have been suggested as major triggering factors for the development of atopic dermatitis. Numerous studies support the association of hygiene hypothesis in allergic immune disorders that a lack of early childhood exposure to diverse microorganism increases susceptibility to allergic diseases. Among the symbiotic microorganisms (e.g. gut flora or probiotics), probiotics confer health benefits through multiple action mechanisms including modification of immune response in gut associated lymphoid tissue (GALT). Although many human clinical trials and mouse studies demonstrated the beneficial effects of probiotics in diverse immune disorders, this effect is strain specific and needs to apply specific probiotics for specific allergic diseases. Herein, we briefly review the diverse functions and regulation mechanisms of probiotics in diverse disorders.

Keywords

References

  1. Sanders, M. E. 2008. Probiotics: definition, sources, selection, and uses. Clin. Infect. Dis. 46 Suppl 2: S58-61. https://doi.org/10.1086/523341
  2. Feleszko, W., J. Jaworska, R. D. Rha, S. Steinhausen, A. Avagyan, A. Jaudszus, B. Ahrens, D. A. Groneberg, U. Wahn, and E. Hamelmann. 2007. Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin. Exp. Allergy 37:498-505. https://doi.org/10.1111/j.1365-2222.2006.02629.x
  3. Miraglia del Giudice, M. Jr., M. G. De Luca, and C. Capristo. 2002. Probiotics and atopic dermatitis. A new strategy in atopic dermatitis. Dig. Liver Dis. 34 Suppl 2: S68-71. https://doi.org/10.1016/S1590-8658(02)80169-4
  4. Sheil, B., F. Shanahan, and L. O'Mahony. 2007. Probiotic effects on inflammatory bowel disease. J. Nutr. 137(3 Suppl2): 819S-824S. https://doi.org/10.1093/jn/137.3.819S
  5. Leung, D. Y., M. Boguniewicz, M. D. Howell, I. Nomura, and Q. A. Hamid. 2004. New insights into atopic dermatitis. J. Clin. Invest. 113: 651-657. https://doi.org/10.1172/JCI21060
  6. Leung, D. Y., N. Jain, and H. L. Leo. 2003. New concepts in the pathogenesis of atopic dermatitis. Curr. Opin. Immunol.15: 634-638. https://doi.org/10.1016/j.coi.2003.09.009
  7. Okada, H., C. Kuhn, H. Feillet, and J. F. Bach. 2010. The 'hygiene hypothesis' for autoimmune and allergic diseases: an update. Clin. Exp. Immunol. 160: 1-9.
  8. Atherton, D. J. 2003. Topical corticosteroids in atopic dermatitis. BMJ 327: 942-943. https://doi.org/10.1136/bmj.327.7421.942
  9. Jia, W., H. Li, L. Zhao, and J. K. Nicholson. 2008. Gut microbiota: a potential new territory for drug targeting. Nat. Rev. Drug Discov. 7: 123-129. https://doi.org/10.1038/nrd2505
  10. Bach, J. F. 2002. The effect of infections on susceptibility to autoimmune and allergic diseases. N. Engl. J. Med. 347:911-920. https://doi.org/10.1056/NEJMra020100
  11. Maggi, E. 1998. The TH1/TH2 paradigm in allergy. Immunotechnology 3: 233-244. https://doi.org/10.1016/S1380-2933(97)10005-7
  12. Rautava, S., O. Ruuskanen, A. Ouwehand, S. Salminen, and E. Isolauri. 2004. The hygiene hypothesis of atopic disease-- an extended version. J. Pediatr. Gastroenterol. Nutr. 38:378-388. https://doi.org/10.1097/00005176-200404000-00004
  13. Shreiner, A., G. B. Huffnagle, and M. C. Noverr. 2008. The "Microflora Hypothesis" of Allergic Disease. In GI Microbiota and Regulation of the Immune System. Springer, New York, USA. pp.113-134
  14. Turnbaugh, P. J., R. E. Ley, M. Hamady, C. M. Fraser-Liggett, R. Knight, and J. I. Gordon. 2007. The human microbiome project. Nature 449: 804-810. https://doi.org/10.1038/nature06244
  15. Human Microbiome Jumpstart Reference Strains Consortium, K. E. Nelson, G. M. Weinstock, S. K. Highlander, K. C. Worley, H. H. Creasy, J. R. Wortman, D. B. Rusch, M. Mitreva, E. Sodergren, A. T. Chinwalla, M. Feldgarden, D. Gevers, B. J. Haas, R. Madupu, D. V. Ward, B. W. Birren, R. A. Gibbs, B. Methe, J. F. Petrosino, R. L. Strausberg, G. G. Sutton, O. R. White, R. K. Wilson, S. Durkin, M. G. Giglio, S. Gujja, C. Howarth, C. D. Kodira, N. Kyrpides, T. Mehta, D. M. Muzny, M. Pearson, K. Pepin, A. Pati, X. Qin, C. Yandava, Q. Zeng, L. Zhang, A. M. Berlin, L. Chen, T. A. Hepburn, J. Johnson, J. McCorrison, J. Miller, P. Minx, C. Nusbaum, C. Russ, S. M. Sykes, C. M. Tomlinson, S. Young, W. C. Warren, J. Badger, J. Crabtree, V. M. Markowitz, J. Orvis, A. Cree, S. Ferriera, L. L. Fulton, R. S. Fulton, M. Gillis, L. D. Hemphill, V. Joshi, C. Kovar, M. Torralba, K. A. Wetterstrand, A. Abouellleil, A. M. Wollam, C. J. Buhay, Y. Ding, S. Dugan, M. G. FitzGerald, M. Holder, J. Hostetler, S. W. Clifton, E. Allen-Vercoe, A. M. Earl, C. N. Farmer, K. Liolios, M. G. Surette, Q. Xu, C. Pohl, K. Wilczek-Boney, and D. Zhu. 2010. A catalog of reference genomes from the human microbiome. Science 328: 994-999. https://doi.org/10.1126/science.1183605
  16. Tlaskalova-Hogenova, H., R. Stepankova, H. Kozakova, T. Hudcovic, L. Vannucci, L. Tuckova, P. Rossmann, T. Hrncir, M. Kverka, Z. Zakostelska, K. Klimesova, J. Pribylova, J. Bartova, D. Sanchez, P. Fundova, D. Borovska, D. Srutkova, Z. Zidek, M. Schwarzer, P. Drastich, and D. P. Funda. 2011. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell. Mol. Immunol. 8: 110-120. https://doi.org/10.1038/cmi.2010.67
  17. Human Microbiome Project Consortium. 2012. A framework for human microbiome research. Nature 486: 215-221. https://doi.org/10.1038/nature11209
  18. Cho, I., and M. J. Blaser. 2012. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13: 260-270. https://doi.org/10.1038/nrg3182
  19. Flohr, C., D. Pascoe, and H. C. Williams. 2005. Atopic dermatitis and the 'hygiene hypothesis': too clean to be true? Br. J. Dermatol. 152: 202-216. https://doi.org/10.1111/j.1365-2133.2004.06436.x
  20. Gibbs, S., H. Surridge, R. Adamson, B. Cohen, G. Bentham, and R. Reading. 2004. Atopic dermatitis and the hygiene hypothesis: a case-control study. Int. J. Epidemiol. 33: 199-207. https://doi.org/10.1093/ije/dyg267
  21. Kalliomaki, M., P. Kirjavainen, E. Eerola, P. Kero, S. Salminen, and E. Isolauri. 2001. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J. Allergy Clin. Immunol. 107: 129-134. https://doi.org/10.1067/mai.2001.111237
  22. Penders, J., C. Thijs, P. A. van den Brandt, I. Kummeling, B. Snijders, F. Stelma, H. Adams, R. van Ree, and E. E. Stobberingh. 2007. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 56: 661-667. https://doi.org/10.1136/gut.2006.100164
  23. Kendler, M., W. Uter, A. Rueffer, R. Shimshoni, and E. Jecht. 2006. Comparison of fecal microflora in children with atopic eczema/dermatitis syndrome according to IgE sensitization to food. Pediatr. Allergy Immunol. 17: 141-147. https://doi.org/10.1111/j.1399-3038.2005.00371.x
  24. Ouwehand, A. C. 2007. Antiallergic effects of probiotics. J. Nutr. 137(3 Suppl 2): 794S-797S. https://doi.org/10.1093/jn/137.3.794S
  25. Turnbaugh, P. J., R. E. Ley, M. A. Mahowald, V. Magrini, E. R. Mardis, and J. I. Gordon. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-1031. https://doi.org/10.1038/nature05414
  26. Ley, R. E., P. J. Turnbaugh, S. Klein, and J. I. Gordon. 2006. Microbial ecology: human gut microbes associated with obesity. Nature 444: 1022-1023. https://doi.org/10.1038/4441022a
  27. Million, M., M. Maraninchi, M. Henry, F. Armougom, H. Richet, P. Carrieri, R. Valero, D. Raccah, B. Vialettes, and D. Raoult. 2012. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int. J. Obes. (Lond). 36: 817-825. https://doi.org/10.1038/ijo.2011.153
  28. Giongo, A., K. A. Gano, D. B. Crabb, N. Mukherjee, L. L. Novelo, G. Casella, J. C. Drew, J. Ilonen, M. Knip, H. Hyöty, R. Veijola, T. Simell, O. Simell, J. Neu, C. H. Wasserfall, D. Schatz, M. A. Atkinson, and E. W. Triplett. 2011. Toward defining the autoimmune microbiome for type 1 diabetes. ISME J. 5:82-91. https://doi.org/10.1038/ismej.2010.92
  29. Ogden, N. S., and L. Bielory. 2005. Probiotics: a complementary approach in the treatment and prevention of pediatric atopic disease. Curr. Opin. Allergy Clin. Immunol. 5: 179-184. https://doi.org/10.1097/01.all.0000162312.64308.fc
  30. Guarner, F., and J. R. Malagelada. 2003. Gut flora in health and disease. Lancet. 361: 512-519. https://doi.org/10.1016/S0140-6736(03)12489-0
  31. Artis, D. 2008. Epithelial-cell recognition ofcommensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 8: 411-420. https://doi.org/10.1038/nri2316
  32. Macdonald, T. T., and G, Monteleone. 2005. Immunity, inflammation, and allergy in the gut. Science 307: 1920-1925. https://doi.org/10.1126/science.1106442
  33. Kelly, D., S. Conway, and R. Aminov. 2005. Commensal gut bacteria: mechanisms of immune modulation. Trends Immunol. 26: 326-333. https://doi.org/10.1016/j.it.2005.04.008
  34. Coombes, J. L., and F. Powrie. 2008. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8: 435-446. https://doi.org/10.1038/nri2335
  35. Rescigno, M., M. Urbano, B. Valzasina, M. Francolini, G. Rotta, R. Bonasio, F. Granucci, J. P. Kraehenbuhl, and P. Ricciardi-Castagnoli. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2: 361-367. https://doi.org/10.1038/86373
  36. Mowat, A. M. 2003. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 3: 331-341. https://doi.org/10.1038/nri1057
  37. O'Hara, A. M., and F. Shanahan. 2006. The gut flora as a forgotten organ. EMBO Rep. 7: 688-693. https://doi.org/10.1038/sj.embor.7400731
  38. Sudo, N., S. Sawamura, K. Tanaka, Y. Aiba, C. Kubo, and Y. Koga. 1997. The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J. Immunol. 159: 1739-1745.
  39. Ostman, S., C. Rask, A. E. Wold, S. Hultkrantz, and E. Telemo. 2006. Impaired regulatory T cell function in germ-free mice. Eur. J. Immunol. 36: 2336-2346. https://doi.org/10.1002/eji.200535244
  40. Kong, H. H. 2011. Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol. Med. 17: 320-328. https://doi.org/10.1016/j.molmed.2011.01.013
  41. Grice, E. A., H. H. Kong, S. Conlan, C. B. Deming, J. Davis, A. C. Young NISC Comparative Sequencing Program, G. G. Bouffard, R. W. Blakesley, P. R. Murray, E. D. Green, M. L. Turner, and J. A. Segre. 2009. Topographical and temporal diversity of the human skin microbiome. Science 324: 1190-1192. https://doi.org/10.1126/science.1171700
  42. Gallo, R. L., and T. Nakatsuji. 2011. Microbial symbiosis with the innate immune defense system of the skin. J. Invest. Dermatol. 131: 1974-1980. https://doi.org/10.1038/jid.2011.182
  43. Kong, H. H., J. Oh, C. Deming, S. Conlan, E. A. Grice, M. A. Beatson, E. Nomicos, E. C. Polley, H. D. Komarow, NISC Comparative Sequence Program, P. R. Murray, M. L. Turner, and J. A. Segre. 2012. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 22: 850-859. https://doi.org/10.1101/gr.131029.111
  44. Lai, Y., A. Di Nardo, T. Nakatsuji, A. Leichtle, Y. Yang, A. L. Cogen, Z. R. Wu, L. V. Hooper, R. R. Schmidt, S. von Aulock, K. A. Radek, C. M. Huang, A. F. Ryan, and R. L. Gallo. 2009. Commensal bacteria regulate Toll-like receptor 3-dependent inflammation after skin injury. Nat. Med. 15: 1377-1382. https://doi.org/10.1038/nm.2062
  45. Naik, S., N. Bouladoux, C. Wilhelm, M. J. Molloy, R. Salcedo, W. Kastenmuller, C. Deming, M. Quinones, L. Koo, S. Conlan, S. Spencer, J. A. Hall, A. Dzutsev, H. Kong, D. J. Campbell, G. Trinchieri, J. A. Segre, and Y. Belkaid. 2012. Compartmentalized control of skin immunity by resident commensals. Science 337: 1115-1119. https://doi.org/10.1126/science.1225152
  46. Ouwehand, A. C., M. Derrien, W. de Vos, K. Tiihonen, and N. Rautonen. 2005. Prebiotics and other microbial substrates for gut functionality. Curr. Opin. Biotechnol. 16: 212-217. https://doi.org/10.1016/j.copbio.2005.01.007
  47. Adlerberth, I., M. Cerquetti, I. Poilane, A. Wold, and A. Collignon. 2000. Mechanisms of Colonisation and Colonisation Resistance of the Digestive Tract Part 1: Bacteria/host Interactions. Microb. Ecol. Health Dis. 2: 223-239.
  48. Fang, H., T. Elina, A. Heikki, and S. Seppo. 2000. Modulation of humoral immune response through probiotic intake. FEMS Immunol. Med. Microbiol. 29: 47-52. https://doi.org/10.1111/j.1574-695X.2000.tb01504.x
  49. Gill, H. S., K. J. Rutherfurd, M. L. Cross, and P. K. Gopal. 2001. Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. Am. J. Clin. Nutr. 74: 833-839. https://doi.org/10.1093/ajcn/74.6.833
  50. Smits, H. H., A. Engering, D. van der Kleij, E. C. de Jong, K. Schipper, T. M. van Capel, B. A. Zaat, M. Yazdanbakhsh, E. A. Wierenga, Y. van Kooyk, and M. L. Kapsenberg. 2005. Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J. Allergy Clin. Immunol. 115: 1260-1267. https://doi.org/10.1016/j.jaci.2005.03.036
  51. Ueno, N., M. Fujiya, S. Segawa, T. Nata, K. Moriichi, H. Tanabe, Y. Mizukami, N. Kobayashi, K. Ito, and Y. Kohgo. 2011. Heat-killed body of lactobacillus brevis SBC8803 ameliorates intestinal injury in a murine model of colitis by enhancing the intestinal barrier function. Inflamm. Bowel Dis. 17: 2235-2250. https://doi.org/10.1002/ibd.21597
  52. Kwon, H. K., C. G. Lee, J. S. So, C. S. Chae, J. S. Hwang, A. Sahoo, J. H. Nam, J. H. Rhee, K. C. Hwang, and S. H. Im. 2012. Generation of regulatory dendritic cells and $CD4^{+}Foxp3^{+}$ T cells by probiotics administration suppresses immune disorders. Proc. Natl. Acad. Sci. U.S.A. 107: 2159-2164.
  53. Winkler, P., D. Ghadimi, J. Schrezenmeir, and J. P. Kraehenbuhl. 2007. Molecular and cellular basis of microflora-host interactions. J. Nutr. 137(3 Suppl 2): 756S-772S. https://doi.org/10.1093/jn/137.3.756S
  54. Fink, L. N., L. H. Zeuthen, G. Ferlazzo, and H. Frøkiaer. 2007. Human antigen-presenting cells respond differently to gut-derived probiotic bacteria but mediate similar strain-dependent NK and T cell activation. FEMS Immunol. Med. Microbiol. 51: 535-546. https://doi.org/10.1111/j.1574-695X.2007.00333.x
  55. Young, S. L., M. A. Simon, M. A. Baird, G. W. Tannock, R. Bibiloni, K. Spencely, J. M. Lane, P. Fitzharris, J. Crane, I. Town, E. Addo-Yobo, C. S. Murray, and A. Woodcock. 2004. Bifidobacterial species differentially affect expression of cell surface markers and cytokines of dendritic cells harvested from cord blood. Clin. Diagn. Lab. Immunol. 11: 686-690.
  56. Zeuthen, L. H., H. R. Christensen, and H. Frøkiaer. 2006. Lactic acid bacteria inducing a weak interleukin-12 and tumor necrosis factor alpha response in human dendritic cells inhibit strongly stimulating lactic acid bacteria but act synergistically with gram-negative bacteria. Clin. Vaccine Immunol. 13: 365-375. https://doi.org/10.1128/CVI.13.3.365-375.2006
  57. Homey, B., M. Steinhoff, T. Ruzicka, and D. Y. Leung. 2006. Cytokines and chemokines orchestrate atopic skin inflammation. J. Allergy Clin. Immunol. 118: 178-189. https://doi.org/10.1016/j.jaci.2006.03.047
  58. Vestergaard, C., N. Kirstejn, B. Gesser, J. T. Mortensen, K. Matsushima, and C. G. Larsen. 2001. IL-10 augments the IFN-gamma and TNF-alpha induced TARC production in HaCaT cells: a possible mechanism in the inflammatory reaction of atopic dermatitis. J. Dermatol. Sci. 26: 46-54. https://doi.org/10.1016/S0923-1811(00)00160-2
  59. Konur, A., U. Schulz, G. Eissner, R. Andreesen, and E. Holler. 2005. Interferon (IFN)-gamma is a main mediator of keratinocyte (HaCaT) apoptosis and contributes to autocrine IFN-gamma and tumour necrosis factor-alpha production. Br. J. Dermatol. 152: 1134-1142. https://doi.org/10.1111/j.1365-2133.2005.06508.x
  60. Pivarcsi, A., and B. Homey. Chemokine networks in atopic dermatitis: traffic signals of disease. Curr. Allergy Asthma Rep. 5: 284-290.
  61. Trautmann, A., M. Akdis, D. Kleemann, F. Altznauer, H. U. Simon, T. Graeve, M. Noll, E. B. Bröcker, K. Blaser, and C. A. Akdis. 2000. T cell-mediated Fas-induced keratinocyte apoptosis plays a key pathogenetic role in eczematous dermatitis. J. Clin. Invest. 106: 25-35. https://doi.org/10.1172/JCI9199
  62. Kalliomäki, M., S. Salminen, H. Arvilommi, P. Kero, P. Koskinen, and E. Isolauri. 2001. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet. 357: 1076-1079. https://doi.org/10.1016/S0140-6736(00)04259-8
  63. Abrahamsson, T. R., T. Jakobsson, M. F. Bottcher, M. Fredrikson, M. C. Jenmalm, B. Bjorksten, and G. Oldaeus. 2007. Probiotics in prevention of IgE-associated eczema: a double-blind, randomized, placebo-controlled trial. J. Allergy Clin. Immunol. 119: 1174-1180. https://doi.org/10.1016/j.jaci.2007.01.007
  64. Wickens, K., P. N. Black, T. V. Stanley, E. Mitchell, P. Fitzharris, G. W. Tannock, G. Purdie, J. Crane Probiotic Study Group. 2008. A differential effect of 2 probiotics in the prevention of eczema and atopy: a double-blind, randomized, placebo-controlled trial. J. Allergy Clin. Immunol. 122: 788-794. https://doi.org/10.1016/j.jaci.2008.07.011
  65. Soh, S. E., M. Aw, I. Gerez, Y. S. Chong, M. Rauff, Y. P. Ng, H. B. Wong, N. Pai, B. W. Lee, and L. P. Shek. 2009. Probiotic supplementation in the first 6 months of life in at risk Asian infants--effects on eczema and atopic sensitization at the age of 1 year. Clin. Exp. Allergy 39: 571-578. https://doi.org/10.1111/j.1365-2222.2008.03133.x
  66. Kopp, M. V., I. Hennemuth, A. Heinzmann, and R. Urbanek. 2008. Randomized, double-blind, placebo-controlled trial of probiotics forprimary prevention: no clinical effects of Lactobacillus GG supplementation. Pediatrics 121: e850-856. https://doi.org/10.1542/peds.2007-1492
  67. Weston, S., A. Halbert, P. Richmond, and S. L. Prescott. 2005. Effects of probiotics on atopic dermatitis: a randomised controlled trial. Arch. Dis. Child. 90: 892-897. https://doi.org/10.1136/adc.2004.060673
  68. Viljanen, M., E. Savilahti, T. Haahtela, K. Juntunen-Backman, R. Korpela, T. Poussa, T. Tuure, and M. Kuitunen. 2005. Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy 60: 494-500. https://doi.org/10.1111/j.1398-9995.2004.00514.x
  69. Sistek, D., R. Kelly, K. Wickens, T. Stanley, P. Fitzharris, and J. Crane. 2006. Is the effect of probiotics on atopic dermatitis confined to food sensitized children? Clin. Exp. Allergy36 :629-633. https://doi.org/10.1111/j.1365-2222.2006.02485.x
  70. Fölster-Holst, R., F. Müller, N. Schnopp, D. Abeck, I. Kreiselmaier, T. Lenz, von U. Rüden, J. Schrezenmeir, E. Christophers, and M. Weichenthal. 2006. Prospective, randomized controlled trial on Lactobacillus rhamnosus in infants with moderate to severe atopic dermatitis. Br. J. Dermatol. 155: 1256-1261. https://doi.org/10.1111/j.1365-2133.2006.07558.x
  71. Chen, Y. S., R. L. Jan, Y. L. Lin, H. H. Chen, and J. Y. Wang. 2010. Randomized placebo-controlled trial of lactobacillus on asthmatic children with allergic rhinitis. Pediatr. Pulmonol. 45: 1111-1120. https://doi.org/10.1002/ppul.21296
  72. Sawada, J., H. Morita, A. Tanaka, S. Salminen, F. He, and H. Matsuda. 2007. Ingestion of heat-treated Lactobacillus rhamnosus GG prevents development of atopic dermatitis in NC/Nga mice. Clin. Exp. Allergy 37: 296-303. https://doi.org/10.1111/j.1365-2222.2006.02645.x
  73. Tanaka, A., K. Jung, J. Benyacoub, G. Prioult, N. Okamoto, K. Ohmori, S. Blum, A. Mercenier, and H. Matsuda. 2009. Oral supplementation with Lactobacillus rhamnosus CGMCC1.3724 prevents development of atopic dermatitis in NC/NgaTnd mice possibly by modulating local production of IFN-gamma. Exp. Dermatol. 18: 1022-1027. https://doi.org/10.1111/j.1600-0625.2009.00895.x
  74. Won, T. J., B. Kim, Y. T. Lim, D. S. Song, S. Y. Park, E. S. Park, D. I. Lee, and K. W. Hwang. 2011. Oral administration of Lactobacillus strains from Kimchi inhibits atopic dermatitis in NC/Nga mice. J. Appl. Microbiol. 110: 1195-1202. https://doi.org/10.1111/j.1365-2672.2011.04981.x
  75. Bouma, G., and W. Strober. 2003. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3: 521-533. https://doi.org/10.1038/nri1132
  76. Swidsinski, A., A. Ladhoff, A. Pernthaler, S. Swidsinski, V. Loening-Baucke, M. Ortner, J. Weber, U. Hoffmann, S. Schreiber, M. Dietel, and H. Lochs. 2002. Mucosal flora in inflammatory bowel disease. Gastroenterology 122: 44-54. https://doi.org/10.1053/gast.2002.30294
  77. Favier, C., C. Neut, C. Mizon, A. Cortot, J. F. Colombel, and J. Mizon. 1997. Fecal beta-D-galactosidase production and Bifidobacteria are decreased in Crohn's disease. Dig. Dis. Sci.42: 817-822. https://doi.org/10.1023/A:1018876400528
  78. Gupta, P., H. Andrew, B. S. Kirschner, and S. Guandalini. 2000. Is lactobacillus GG helpful in children with Crohn's disease? Results of a preliminary, open-label study. J. Pediatr. Gastroenterol. Nutr. 31: 453-457. https://doi.org/10.1097/00005176-200010000-00024
  79. Kruis, W., P. Fric, and M. S. Stolte. 2001. Maintenance of remission in ulcerative colitis is equally effective with Escherichia coli Nissle 1917 and with standard mesalamine. Gastroenterology 120(5 Suppl 1): A127. https://doi.org/10.1016/S0016-5085(08)80627-0
  80. Malchow, H. A. 1997. Crohn's disease and Escherichia coli. A new approach in therapy to maintain remission of colonic Crohn's disease? J. Clin. Gastroenterol. 25: 653-658. https://doi.org/10.1097/00004836-199712000-00021
  81. Gionchetti, P., F. Rizzello, A. Venturi, P. Brigidi, D. Matteuzzi, G. Bazzocchi, G. Poggioli, M. Miglioli, and M. Campieri. 2000. Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo- controlled trial. Gastroenterology 119: 305-309. https://doi.org/10.1053/gast.2000.9370
  82. Venturi, A., P. Gionchetti, F. Rizzello, R. Johansson, E. Zucconi, P. Brigidi, D. Matteuzzi, and M. Campieri. 1999. Impact on the composition of the faecal flora by a new probiotic preparation: preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment. Pharmacol. Ther.13: 1103-1108. https://doi.org/10.1046/j.1365-2036.1999.00560.x
  83. O'Mahony, L., M. Feeney, S. O'Halloran, L. Murphy, B. Kiely, J. Fitzgibbon, G. Lee, G. O'Sullivan, F. Shanahan, and J. K. Collins. 2001. Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice. Aliment. Pharmacol. Ther. 15: 1219-1225. https://doi.org/10.1046/j.1365-2036.2001.01027.x
  84. Sheil, B., J. MacSharry, L. O'Callaghan, A. O'Riordan, A. Waters, J, Morgan, J. K. Collins, L. O'Mahony, and F. Shanahan. 2006. Role of interleukin (IL-10) in probioticmediated immune modulation: an assessment in wild-type and IL-10 knock-out mice. Clin. Exp. Immunol. 144: 273-280. https://doi.org/10.1111/j.1365-2249.2006.03051.x
  85. Sheil, B., J. McCarthy, L. O'Mahony, M. W. Bennett, P. Ryan, J. J. Fitzgibbon, B. Kiely, J. K. Collins, and F. Shanahan. 2004. Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis. Gut 53: 694-700. https://doi.org/10.1136/gut.2003.027789
  86. Madsen, K. L., J. S. Doyle, L. D. Jewell, M. M. Tavernini, and R. N. Fedorak. 1999. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116: 1107-1114. https://doi.org/10.1016/S0016-5085(99)70013-2
  87. Schultz, M., C. Veltkamp, L. A. Dieleman, W. B. Grenther, P. B. Wyrick, S. L. Tonkonogy, and R. B. Sartor. 2002. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm. Bowel Dis. 8: 71-80. https://doi.org/10.1097/00054725-200203000-00001
  88. Khoruts, A., and M. J. Sadowsky. 2011. Therapeutic transplantation of the distal gut microbiota. Mucosal Immunol. 4: 4-7. https://doi.org/10.1038/mi.2010.79
  89. Delzenne, N. M., A. M. Neyrinck, F. Bäckhed, and P. D. Cani. 2011. Targeting gut microbiota in obesity: effects of prebiotics and probiotics. Nat. Rev. Endocrinol. 7: 639-646. https://doi.org/10.1038/nrendo.2011.126

Cited by

  1. Man and his spaceships : Vehicles for extraterrestrial colonization? vol.2, pp.6, 2012, https://doi.org/10.4161/mge.23238
  2. Gut Microbes and Host Physiology: What Happens When You Host Billions of Guests? vol.5, pp.None, 2012, https://doi.org/10.3389/fendo.2014.00091
  3. External Influence of Early Childhood Establishment of Gut Microbiota and Subsequent Health Implications vol.2, pp.None, 2012, https://doi.org/10.3389/fped.2014.00109
  4. Gut microbiota disturbance during antibiotic therapy : A multi-omic approach vol.5, pp.1, 2014, https://doi.org/10.4161/gmic.27128
  5. A novel SCFA receptor, the microbiota, and blood pressure regulation vol.5, pp.2, 2014, https://doi.org/10.4161/gmic.27492
  6. The effects of the microbiota on the host immune system vol.47, pp.8, 2014, https://doi.org/10.3109/08916934.2014.938322
  7. From microbe to man: the role of microbial short chain fatty acid metabolites in host cell biology vol.307, pp.11, 2012, https://doi.org/10.1152/ajpcell.00228.2014
  8. Protective effect of probiotics in the treatment of infantile eczema vol.9, pp.5, 2012, https://doi.org/10.3892/etm.2015.2299
  9. The role of short-chain fatty acid on blood pressure regulation vol.25, pp.5, 2012, https://doi.org/10.1097/mnh.0000000000000246
  10. Origination, change, and modulation of geriatric disease-related gut microbiota during life vol.102, pp.19, 2012, https://doi.org/10.1007/s00253-018-9264-2
  11. Cell surface polysaccharides of Bifidobacterium bifidum induce the generation of Foxp3+ regulatory T cells vol.3, pp.28, 2012, https://doi.org/10.1126/sciimmunol.aat6975
  12. The Post-amyloid Era in Alzheimer's Disease: Trust Your Gut Feeling vol.11, pp.None, 2012, https://doi.org/10.3389/fnagi.2019.00143
  13. Dysbiosis of the Gut Microbiome in Lung Cancer vol.9, pp.None, 2012, https://doi.org/10.3389/fcimb.2019.00112
  14. Targeting Infectious Agents as a Therapeutic Strategy in Alzheimer’s Disease vol.34, pp.7, 2012, https://doi.org/10.1007/s40263-020-00737-1
  15. Autism Spectrum Disorder and Medical Cannabis: Review and Clinical Experience vol.35, pp.None, 2020, https://doi.org/10.1016/j.spen.2020.100833
  16. Probiotic mixture reduces gut inflammation and microbial dysbiosis in children with atopic dermatitis vol.62, pp.3, 2012, https://doi.org/10.1111/ajd.13644