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Development of Gut Microbiota in a Mouse Model of Ovalbumin-induced Allergic Diarrhea under Sub-barrier System

  • Wang, Juan-Hong (Laboratory of Gastrointestinal Microbiology, Nanjing Agricultural University) ;
  • Fan, Song-Wei (Laboratory of Gastrointestinal Microbiology, Nanjing Agricultural University) ;
  • Zhu, Wei-Yun (Laboratory of Gastrointestinal Microbiology, Nanjing Agricultural University)
  • Received : 2012.09.14
  • Accepted : 2012.12.14
  • Published : 2013.04.01

Abstract

This study aimed to present a mouse model of ovalbumin (OVA) induced allergic diarrhea under a sub-barrier system and investigate the development of gut microbiota in this model. Male BALB/c mice were systemically sensitized with OVA or sham-sensitized with saline, and followed by oral OVA intubation, leading to OVA-specific acute diarrhea. Compared with sham-sensitized mice, sera OVA-specific IgG1 and total IgE in OVA-sensitized mice were dramatically elevated, and the number of mast cells was greatly increased in the jejunum of the OVA-sensitized mice. Principle component analysis of the DGGE profile showed that samples from group of OVA-sensitized mice and group of sham-sensitized mice were scattered into two different regions. Real-time PCR analysis showed that the number of 16S rRNA gene copies of Lactobacillus in the colon of OVA-sensitized mice decreased significantly, while there was no significant difference in the number of Bifidobacterium and total bacteria. In conclusion, OVA-specific allergic diarrhea was successfully induced under a sub-barrier system, and changes of allergic reactions during induction was coupled with changes in gut microbiota, especially the number of colonic Lactobacillus, but the role of gut microbiota in the development of food allergic reactions needs to be further evaluated.

Keywords

References

  1. Bashir, M. E., S. Louie, H. N. Shi and C. Nagler-Anderson. 2004. Toll-like receptor 4 signaling by intestinal microbes influences susceptibility to food allergy. J. Immunol. 172:6978-6987. https://doi.org/10.4049/jimmunol.172.11.6978
  2. Beckstead, J. H., P. S. Halverson, C. A. Ries and D. F. Bainton. 1981. Enzyme histochemistry and immunohistochemistry on biopsy specimens of pathologic human bone marrow. Blood. 57:1088-1098.
  3. Bischoff, S. C. and S. Kramer. 2007. Human mast cells, bacteria and intestinal immunity. Immunol. Rev. 217:329-337. https://doi.org/10.1111/j.1600-065X.2007.00523.x
  4. Bjorksten, B., P. Naaber, E. Sepp and M. Mikelsaar. 1999. The intestinal microflora in allergic Estonian and Swedish two-year-old-children. Clin. Exp. Allergy 29:342-346. https://doi.org/10.1046/j.1365-2222.1999.00560.x
  5. Bjorksten, B., E. Sepp, K. Julge, T. Voor and M. Mikelsaar. 2001. Allergy development and the intestinal microflora during the first year of life. J. Allergy Clin. Immun. 108:516-520. https://doi.org/10.1067/mai.2001.118130
  6. Bottcher, M. F., E. K. Nordin, A. Sandin, T. Midtvedt and B. Bjorksten. 2000. Microflora-associated characteristics in faeces from allergic and non-allergic infants. Clin. Exp. Allergy 30:1590-1596.
  7. Brandt, E. B., R. T. Strait, D. Hershko, Q. Wang, E. E. Muntel, T. A. Scribner, N. Zimmermann, F. D. Finkelman and M. E. Rothenberg. 2003. Mast cells are required for experimental oral allergen-induced diarrhea. J. Clin. Invest. 2:1666-1677.
  8. Brandt, E. B., A. Munitz, T. Orekov, M. K. Mingler, M. McBride, F. D. Finkelman and M. E. Rothenberg. 2009. Targeting IL-4/IL-13 signaling to alleviate oral allergen-induced diarrhea.J. Allergy Clin. Immun. 123:53-58. https://doi.org/10.1016/j.jaci.2008.10.001
  9. Forbes, E. E., K. Groschwitz, J. P. Abonia, E. B. Brandt, E. Cohen, C. Blanchard, R. Ahrens, L. Seidu, A. McKenzie, R. Strait, F. D. Finkelman, P. S. Foster, K. I. Matthaei, M. E. Rothenberg and S. P. Hogan. 2008. IL-9- and mast cell-mediated intestinal permeability predisposes to oral antigen hypersensitivity. J. Exp. Med. 205:897-913. https://doi.org/10.1084/jem.20071046
  10. Forsythe, P., M. D. Inman and J. Bienenstock. 2007. Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice. Am. J. Respir. Crit. Care Med. 175:561-569. https://doi.org/10.1164/rccm.200606-821OC
  11. Helm, R. M., R. W. Ermel and O. L. Frick. 2003. Nonmurine animal models of food allergy. Environ. Health Perspect. 111:239-244. https://doi.org/10.1289/ehp.5705
  12. Hougee, S., A. J. Vriesema, S. C. Wijering, L. M. Knippels, G. Folkerts, F. P. Nijkamp, J. Knol and J. Garssen. 2010. Oral treatment with probiotics reduces allergic symptoms in ovalbumin-sensitized mice: a bacterial strain comparative study. Int. Arch. Allergy Immunol. 151:107-117. https://doi.org/10.1159/000236000
  13. Iliev, I. D., M. Tohno, D. Kurosaki, T. Shimosato, F. He, M. Hosoda, T. Saito and H. Kitazawa. 2008. Immunostimulatory oligodeoxynucleotide containing TTTCGTTT motif from Lactobacillus rhamnosus GG dna potentially suppresses OVA-specific IgE production in mice. Scand. J. Immunol. 67:370-376. https://doi.org/10.1111/j.1365-3083.2008.02080.x
  14. Johansson, M. A., Y. M. Sjogren, J. O. Persson, C. Nilsson and E. Sverremark-Ekstrom. 2011. Early colonization with a group of Lactobacilli decreases the risk for allergy at five years of age despite allergic heredity. PLoS One. 6:e23031. https://doi.org/10.1371/journal.pone.0023031
  15. Khafipour, E., S. Li, J. C. Plaizier and D. O. Krause. 2009. Rumen microbiome composition determined using two nutritional models of subacute ruminal acidosis. Appl. Environ. Microbiol. 75:7115-7124. https://doi.org/10.1128/AEM.00739-09
  16. Kim, J. Y., Y. O. Choi and G. E. Ji. 2008. Effect of oral probiotics (Bifidobacterium lactis AD011 and Lactobacillus acidophilus AD031) administration on ovalbumin-induced food allergy mouse model. J. Microbiol. Biotechnol. 18:1393-1400.
  17. Kweon, M. N., M. Yamamoto, M. Kajiki, I. Takahashi and H. Kiyono. 2000. Systemically derived large intestinal CD4(+) Th2 cells play a central role in STAT6-mediated allergic diarrhea. J. Clin. Invest. 106:199-206. https://doi.org/10.1172/JCI8490
  18. Li, F., J. Z. Wu and Y. Li. 2003. Experience of breeding nude mice in laminar flow cabinet. Lab. Anim. Sci. Adm. 20:52-54.
  19. Li, H. and W. Chen. 2005. Breeding diabetes scid mice with streamline cabinet. Lab. Anim. Sci. Adm. 22:54-55.
  20. Matsuki, T., K. Watanabe, J. Fujimoto, T. Takada and R. Tanaka. 2004. Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl. Environ. Microbiol. 70:7220-7228. https://doi.org/10.1128/AEM.70.12.7220-7228.2004
  21. Muyzer, G., E. C. de Waal and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
  22. Nubel, U., B. Engelen, A. Felske, J. Snaidr, A. Wieshuber, R. I. Amann, W. Ludwig and H. Backhaus. 1996. Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J. Bacteriol.178:5636-5643.
  23. Prioult, G. and C. Nagler-Anderson. 2005. Mucosal immunity and allergic responses: lack of regulation and/or lack of microbial stimulation. Immunol. Rev. 206:204-218. https://doi.org/10.1111/j.0105-2896.2005.00277.x
  24. Sanguinetti, C. J., D. Dias Neto and A. J. Simpson. 1994. Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17:914-921.
  25. Schouten, B., B. C. van Esch, G. A. Hofman, S. A. van Doorn, J. Knol, A. J. Nauta, J. Garssen, L. E. Willemsen and L. M. Knippels. 2009. Cow milk allergy symptoms are reduced in mice fed dietary synbiotics during oral sensitization with whey. J. Nutr. 139:1398-1403. https://doi.org/10.3945/jn.109.108514
  26. Sicherer, S. H. and H. A. Sampson. 2006. Food allergy. J. Allergy Clin. Immunol. 117:S470-S475. https://doi.org/10.1016/j.jaci.2005.05.048
  27. Sjogren, Y. M., M. C. Jenmalmw, M. F. Bottcher, B. Bjorksten and E. Sverremark-Ekstrom. 2009. Altered early infant gut microbiota in children developing allergy up to 5 years of age. Clin. Exp. Allergy 39:518-526. https://doi.org/10.1111/j.1365-2222.2008.03156.x
  28. Strachan, D. P. 1989. Hay fever, hygiene, and household size. BMJ. 299:1295-1260. https://doi.org/10.1136/bmj.299.6711.1295
  29. Sunada, Y., S. Nakamura and C. Kamei. 2007. Effects of Lactobacillus acidophilus strain L-55 on experimental allergic rhinitis in BALB/c mice. Biol. Pharm. Bull. 30:2163-2166. https://doi.org/10.1248/bpb.30.2163
  30. Suzuki, M. T., L. T. Taylor and E. F. DeLong. 2000. Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5'-nuclease assays. Appl. Environ. Microbiol. 66:4605-4614. https://doi.org/10.1128/AEM.66.11.4605-4614.2000
  31. Takahashi, N., H. Kitazawa, N. Iwabuchi, J. Z. Xiao, K. Miyaji, K. Iwatsuki and T. Saito. 2006. Immunostimulatory oligodeoxynucleotide from Bifidobacterium Longum suppresses Th2 immune responses in a murine model. Clin. Exp. Immunol. 145:130-138. https://doi.org/10.1111/j.1365-2249.2006.03111.x
  32. Wang, M., C. Karlsson, C. Olsson, I. Adlerberth, A. E. Wold, D. P. Strachan, P. M. Martricardi, N. Aberg, M. R. Perkin, S. Tripodi, A. R. Coates, B. Hesselmar, R. Saalman, G. Molin and S. Ahrne. 2008. Reduced diversity in the early fecal microbiota of infants with atopic eczema. J. Allergy Clin. Immunol. 121:129-134. https://doi.org/10.1016/j.jaci.2007.09.011
  33. 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
  34. Zoetendal, E. G., A. D. Akkermans and W. M. De Vos. 1998. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl. Environ. Microbiol. 64:3854-3859.

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