Advertisement

Journal of Microbiology

, Volume 56, Issue 4, pp 272–279 | Cite as

A murine colitis model developed using a combination of dextran sulfate sodium and Citrobacter rodentium

  • Jin-Il Park
  • Sun-Min Seo
  • Jong-Hyung Park
  • Hee-Yeon Jeon
  • Jun-Young Kim
  • Seung-Hyun Ryu
  • Yang-Kyu Choi
Microbial Pathogenesis and Host-Microbe Interaction

Abstract

Adult mice were treated with dextran sulfate sodium (DSS) and infected with Citrobacter rodentium for developing a novel murine colitis model. C57BL/6N mice (7-week-old) were divided into four groups. Each group composed of control, dextran sodium sulfate-treated (DSS), C. rodentium-infected (CT), and DSS-treated and C. rodentium-infected (DSS-CT) mice. The DSS group was administered 1% DSS in drinking water for 7 days. The CT group was supplied with normal drinking water for 7 days and subsequently infected with C. rodentium via oral gavage. The DSS-CT group was supplied with 1% DSS in drinking water for 7 days and subsequently infected with C. rodentium via oral gavage. The mice were sacrificed 10 days after the induction of C. rodentium infection. The DSS-CT group displayed significantly shorter colon length, higher spleen to body weight ratio, and higher histopathological score compared to the other three groups. The mRNA expression levels of tumor necrosis factor (TNF)-α and interferon (INF)-γ were significantly upregulated; however, those of interleukin (IL)-6 and IL-10 were significantly downregulated in the DSS-CT group than in the control group. These results demonstrated that a combination of low DSS concentration (1%) and C. rodentium infection could effectively induce inflammatory bowel disease (IBD) in mice. This may potentially be used as a novel IBD model, in which colitis is induced in mice by the combination of a chemical and a pathogen.

Keywords

Citrobacter rodentium colitis dextran sulfate sodium 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

12275_2018_7504_MOESM1_ESM.pdf (875 kb)
Supplementary material, approximately 875 KB.

References

  1. Alipour, M., Lou, Y., Zimmerman, D., Bording-Jorgensen, M.W., Sergi, C., Liu, J.J., and Wine, E. 2013. A balanced IL-1β activity is required for host response to Citrobacter rodentium infection. PLoS One 8, e80656.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Andres, P.G. and Friedman, L.S. 1999. Epidemiology and the natural course of inflammatory bowel disease. Gastroenterol. Clin. North Am. 28, 255–281.CrossRefPubMedGoogle Scholar
  3. Axelsson, L.G., Landström, E., Goldschmidt, T.J., Grönberg, A., and Bylund-Fellenius, A.C. 1996. Dextran sulfate sodium (DSS) induced experimental colitis in immunodeficient mice: effects in CD4+-cell depleted, athymic and NK-cell depleted SCID mice. Inflamm. Res. 45, 181–191.CrossRefPubMedGoogle Scholar
  4. Bauer, C., Duewell, P., Mayer, C., Lehr, H.A., Fitzgerald, K.A., Dauer, M., Tschopp, J., Endres, S., Latz, E., and Schnurr, M. 2010. Colitis induced in mice with dextran sulfate sodium (DSS) is mediated by the NLRP3 inflammasome. Gut 59, 1192–1199.CrossRefPubMedGoogle Scholar
  5. Casati, J. and Toner, B.B. 2000. Psychosocial aspects of inflammatory bowel disease. Biomed. Pharmacother. 54, 388–393.CrossRefPubMedGoogle Scholar
  6. Chassaing, B., Aitken, J.D., Malleshappa, M., and Vijay-Kumar, M. 2014. Dextran sulfate sodium (DSS)-induced colitis in mice. Curr. Protoc. Immunol. 104, Unit 15.25.Google Scholar
  7. Deng, W., Li, Y., Vallance, B.A., and Finlay, B.B. 2001. Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect. Immun. 69, 6323–6335.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Eckmann, L. 2006. Animal models of inflammatory bowel disease: lessons from enteric infections. Ann. N. Y. Acad. Sci. 1072, 28–38.CrossRefPubMedGoogle Scholar
  9. Flynn, J.L., Chan, J.M., Triebold, K.J., Dalton, D.K., Stewart, T.A., and Bloom, B.R. 1993. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178, 2249–2254.CrossRefPubMedGoogle Scholar
  10. Gibson, D.L., Ma, C., Rosenberger, C.M., Bergstrom, K.S., Valdez, Y., Huang, J.T., Khan, M.A., and Vallance, B.A. 2008. Toll-like receptor 2 plays a critical role in maintaining mucosal integrity during Citrobacter rodentium-induced colitis. Cell. Microbiol. 10, 388–403.CrossRefPubMedGoogle Scholar
  11. Hanauer, S.B. 2006. Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm. Bowel Dis. 12 Suppl 1, S3–S9.CrossRefPubMedGoogle Scholar
  12. Hirono, I., Kuhara, K., Yamaji, T., Hosaka, S., and Golberg, L. 1983. Carcinogenicity of dextran sulfate sodium in relation to its molecular weight. Cancer Lett. 18, 29–34.CrossRefPubMedGoogle Scholar
  13. Hoshi, O., Iwanaga, T., and Fujino, M.A. 1996. Selective uptake of intraluminal dextran sulfate sodium and senna by macrophages in the cecal mucosa of the guinea pig. J. Gastroenterol. 31, 189–198.CrossRefPubMedGoogle Scholar
  14. Iwanaga, T., Hoshi, O., Han, H., and Fujita, T. 1994. Morphological analysis of acute ulcerative colitis experimentally induced by dextran sulfate sodium in the guinea pig: some possible mechanisms of cecal ulceration. J. Gastroenterol. 29, 430–438.CrossRefPubMedGoogle Scholar
  15. Kim, J.J., Shajib, M.S., Manocha, M.M., and Khan, W.I. 2012. Investigating intestinal inflammation in DSS-induced model of IBD. J. Vis. Exp. 60, e3678.Google Scholar
  16. Kitajima, S., Takuma, S., and Morimoto, M. 2000. Histological analysis of murine colitis induced by dextran sulfate sodium of different molecular weights. Exp. Anim. 49, 9–15.CrossRefPubMedGoogle Scholar
  17. Knod, J.L., Crawford, K., Dusing, M., and Frischer, J.S. 2014. Mouse strain influences angiogenic response to dextran sodium sulfate-induced colitis. J. Surg. Res. 190, 47–54.CrossRefPubMedGoogle Scholar
  18. Kwon, K.H., Murakami, A., Tanaka, T., and Ohigashi, H. 2005. Dietary rutin, but not its aglycone quercetin, ameliorates dextran sulfate sodium-induced experimental colitis in mice: attenuation of pro-inflammatory gene expression. Biochem. Pharmacol. 69, 395–406.CrossRefPubMedGoogle Scholar
  19. Luperchio, S.A. and Schauer, D.B. 2001. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 3, 333–340.CrossRefPubMedGoogle Scholar
  20. Maaser, C., Housley, M.P., Iimura, M., Smith, J.R., Vallance, B.A., Finlay, B.B., Schreiber, J.R., Varki, N.M., Kagnoff, M.F., and Eckmann, L. 2004. Clearance of Citrobacter rodentium requires B cells but not secretory immunoglobulin A (IgA) or IgM antibodies. Infect. Immun. 72, 3315–3324.CrossRefPubMedPubMedCentralGoogle Scholar
  21. MacDonald, T.T., Frankel, G., Dougan, G., Goncalves, N.S., and Simmons, C. 2003. Host defences to Citrobacter rodentium. Int. J. Med. Microbiol. 293, 87–93.CrossRefPubMedGoogle Scholar
  22. Moore, K.W., de Waal Malefyt, R., Coffman, R.L., and O’Garra, A. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683–765.CrossRefPubMedGoogle Scholar
  23. Mundy, R., MacDonald, T.T., Dougan, G., Frankel, G., and Wiles, S. 2005. Citrobacter rodentium of mice and man. Cell. Microbiol. 7, 1697–1706.CrossRefPubMedGoogle Scholar
  24. Ohkusa, T., Okayasu, I., Tokoi, S., Araki, A., and Ozaki, Y. 1995. Changes in bacterial phagocytosis of macrophages in experimental ulcerative colitis. Digestion 56, 159–164.CrossRefPubMedGoogle Scholar
  25. Okayasu, I., Hatakeyama, S., Yamada, M., Ohkusa, T., Inagaki, Y., and Nakaya, R. 1990. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98, 694–702.CrossRefPubMedGoogle Scholar
  26. Ouyang, N., Zhu, C., Zhou, D., Nie, T., Go, M.F., Richards, R.J., and Rigas, B. 2012. MC-12, an annexin A1-based peptide, is effective in the treatment of experimental colitis. PLoS One 7, e41585.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Perše, M. and Cerar, A. 2012. Dextran sodium sulphate colitis mouse model: traps and tricks. J. Biomed. Biotechnol. 2012, 718617.Google Scholar
  28. Randhawa, P.K., Singh, K., Singh, N., and Jaggi, A.S. 2014. A review on chemical-induced inflammatory bowel disease models in rodents. Korean J. Physiol. Pharmacol. 18, 279–288.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Rath, H.C., Herfarth, H.H., Ikeda, J.S., Grenther, W.B., Hamm, T.E. Jr., Balish, E., Taurog, J.D., Hammer, R.E., Wilson, K.H., and Sartor, R.B. 1996. Normal luminal bacteria, especially bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J. Clin. Invest. 98, 945–953.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Ryu, S.H., Park, J.H., Choi, S.Y., Jeon, H.Y., Park, J.I., Kim, J.Y., Ham, S.H., and Choi, Y.K. 2016. The probiotic Lactobacillus prevents Citrobacter rodentium-induced murine colitis in a TLR2-dependent manner. J. Microbiol. Biotechnol. 26, 1333–1340.CrossRefPubMedGoogle Scholar
  31. Sang, L., Chang, B., Zhu, J., Yang, F., Li, Y., Jiang, X., Sun, X., Lu., C., and Wang, D. 2016. Dextran sulfate sodium-induced acute experimental colitis in C57BL/6 mice is mitigated by selenium. Int. Immunopharmacol. 39, 359–368.CrossRefPubMedGoogle Scholar
  32. Scheller, J., Chalaris, A., Schmidt-Arras, D., and Rose-John, S. 2011. The pro-and anti-inflammatory properties of the cytokine interleukin-6. Biochim. Biophys. Acta 1813, 878–888.CrossRefPubMedGoogle Scholar
  33. Simmons, C.P., Goncalves, N.S., Ghaem-Maghami, M., Bajaj-Elliott, M., Clare, S., Neves, B., Frankel, G., Dougan, G., and MacDonald, T.T. 2002. Impaired resistance and enhanced pathology during infection with a noninvasive, attaching-effacing enteric bacterial pathogen, Citrobacter rodentium, in mice lacking IL-12 or IFN-γ. J. Immunol. 168, 1804–1812.CrossRefPubMedGoogle Scholar
  34. Wu, X., Vallance, B.A., Boyer, L., Bergstrom, K.S., Walker, J., Madsen, K., O’Kusky, J.R., Buchan, A.M., and Jacobson, K. 2008. Saccharomyces boulardii ameliorates Citrobacter rodentium-induced colitis through actions on bacterial virulence factors. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G295–G306.CrossRefPubMedGoogle Scholar
  35. Yamada, M., Ohkusa, T., and Okayasu, I. 1992. Occurrence of dysplasia and adenocarcinoma after experimental chronic ulcerative colitis in hamsters induced by dextran sulphate sodium. Gut 33, 1521–1527.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Yu, D., Zhu, H., Liu, Y., Cao, J., and Zhang, X. 2009. Regulation of proinflammatory cytokine expression in primary mouse astrocytes by coronavirus infection. J. Virol. 83, 12204–12214.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer Nature B.V. 2018

Authors and Affiliations

  • Jin-Il Park
    • 1
    • 2
  • Sun-Min Seo
    • 1
  • Jong-Hyung Park
    • 1
  • Hee-Yeon Jeon
    • 1
    • 3
  • Jun-Young Kim
    • 1
  • Seung-Hyun Ryu
    • 1
    • 4
  • Yang-Kyu Choi
    • 1
  1. 1.Department of Laboratory Animal Medicine, College of Veterinary MedicineKonkuk UniversitySeoulRepublic of Korea
  2. 2.ViroMed Co. Ltd.SeoulRepublic of Korea
  3. 3.Department of Core Research Laboratory, Clinical Research InstituteKyung Hee University Hospital at GangdongSeoulRepublic of Korea
  4. 4.Samjin Pharmaceutical Co., Ltd.SeoulRepublic of Korea

Personalised recommendations