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.
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02 May 2018
In the article by Park <Emphasis Type="Italic">et al.</Emphasis> published in Journal of Microbiology 2018; 56, 272–279, the supplementary data Figs S1 and S2 should be corrected as below. The original article can be found online at <ExternalRef><RefSource>https://doi.org/10.1007/s12275-018-7504-x</RefSource><RefTarget Address="https://doi.org/10.1007/s12275-018-7504-x" TargetType="URL"/></ExternalRef>.
References
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.
Andres, P.G. and Friedman, L.S. 1999. Epidemiology and the natural course of inflammatory bowel disease. Gastroenterol. Clin. North Am. 28, 255–281.
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.
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.
Casati, J. and Toner, B.B. 2000. Psychosocial aspects of inflammatory bowel disease. Biomed. Pharmacother. 54, 388–393.
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.
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.
Eckmann, L. 2006. Animal models of inflammatory bowel disease: lessons from enteric infections. Ann. N. Y. Acad. Sci. 1072, 28–38.
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.
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.
Hanauer, S.B. 2006. Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm. Bowel Dis. 12 Suppl 1, S3–S9.
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.
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.
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.
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.
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.
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.
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.
Luperchio, S.A. and Schauer, D.B. 2001. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 3, 333–340.
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.
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.
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.
Mundy, R., MacDonald, T.T., Dougan, G., Frankel, G., and Wiles, S. 2005. Citrobacter rodentium of mice and man. Cell. Microbiol. 7, 1697–1706.
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.
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.
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.
Perše, M. and Cerar, A. 2012. Dextran sodium sulphate colitis mouse model: traps and tricks. J. Biomed. Biotechnol. 2012, 718617.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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A correction to this article is available at https://doi.org/10.1007/s12275-018-0578-7
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Park, JI., Seo, SM., Park, JH. et al. A murine colitis model developed using a combination of dextran sulfate sodium and Citrobacter rodentium. J Microbiol. 56, 272–279 (2018). https://doi.org/10.1007/s12275-018-7504-x
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DOI: https://doi.org/10.1007/s12275-018-7504-x