Shift Towards Pro-inflammatory Intestinal Bacteria Aggravates Acute Murine Colitis via Toll-like Receptors 2 and 4
Open accessAbstract
BACKGROUND: Gut bacteria trigger colitis in animal models and are suspected to aggravate inflammatory bowel diseases. We have recently reported that Escherichia coli accumulates in murine ileitis and exacerbates small intestinal inflammation via Toll-like receptor (TLR) signaling. METHODOLOGY AND PRINCIPAL FINDINGS: Because knowledge on shifts in the intestinal microflora during colitis is limited, we performed a global survey of the colon flora of C57BL/10 wild-type (wt), TLR2(-/-), TLR4(-/-), and TLR2/4(-/-) mice treated for seven days with 3.5% dextrane-sulfate-sodium (DSS). As compared to wt animals, TLR2(-/-), TLR4(-/-), and TLR2/4(-/-) mice displayed reduced macroscopic signs of acute colitis and the amelioration of inflammation was associated with reduced IFN-gamma levels in mesenteric lymph nodes, lower amounts of neutrophils, and less FOXP3-positive T-cells in the colon in situ. During acute colitis E. coli increased in wt and TLR-deficient mice (P<0.05), but the final numbers reached were significantly lower in TLR2(-/-), TLR4(-/-) and TLR2/4(-/-) animals, as compared to wt controls (P<0.01). Concentrations of Bacteroides/ Prevotella spp., and enterococci did not increase during colitis, but their numbers were significantly reduced in the colon of DSS-treated TLR2/4(-/-) animals (P<0.01). Numbers of lactobacilli and clostridia remained unaffected by colitis, irrespective of the TLR-genotype of mice. Culture-independent molecular analyses confirmed the microflora shifts towards enterobacteria during colitis and showed that the gut flora composition was similar in both, healthy wt and TLR-deficient animals. CONCLUSIONS AND SIGNIFICANCE: DSS-induced colitis is characterized by a shift in the intestinal microflora towards pro-inflammatory Gram-negative bacteria. Bacterial products exacerbate acute inflammation via TLR2- and TLR4-signaling and direct the recruitment of neutrophils and regulatory T-cells to intestinal sites. E. coli may serve as a biomarker for colitis severity and DSS-induced barrier damage seems to be a valuable model to further identify bacterial factors involved in maintaining intestinal homeostasis and to test therapeutic interventions based upon anti-TLR strategies.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Many studies have reported that alterations in the gut microbiota induce both pro- and anti-inflammatory effects in the host.
“Many studies have reported that alterations in the gut microbiota induce both pro- and anti-inflammatory effects in the host.5–7”
From Using Corticosteroids to Reshape the Gut Microbiome: Implications for Inflammatory Bowel Diseases (2015) · cites this paper as [5]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Recognition of Commensal Microflora by Toll-Like Receptors Is Required for Intestinal Homeostasis
Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S., & Medzhitov, R. (2004) · Cell · doi:10.1016/j.cell.2004.07.002 · Cited by 4,251 · see citing works
Podolsky, D. K. (2002) · New England Journal of Medicine · doi:10.1056/nejmra020831 · Cited by 3,183 · see citing works
Darfeuille-Michaud, A., Boudeau, J., Bulois, P., Neut, C., Glasser, A.-L., Barnich, N., Bringer, M.-A., Swidsinski, A., Beaugerie, L., & Colombel, J.-F. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.04.061 · Cited by 1,566 · see citing works
Mucosal flora in inflammatory bowel disease
Swidsinski, A. V., Ladhoff, A., Pernthaler, A., Swidsinski, S., Loening-Baucke, V. A., Ortner, M., Weber, J., Hoffmann, U., Schreiber, S., Dietel, M., et al. (2002) · Gastroenterology · doi:10.1053/gast.2002.30294 · Cited by 1,344 · see citing works
The Immunology of Mucosal Models of Inflammation
Strober, W., Fuss, I. J., & Blumberg, R. S. (2002) · Annual Review of Immunology · doi:10.1146/annurev.immunol.20.100301.064816 · Cited by 1,300 · see citing works
Cario, E., & Podolsky, D. K. (2000) · Infection and Immunity · doi:10.1128/iai.68.12.7010-7017.2000 · Cited by 1,245 · see citing works
Swidsinski, A., Weber, J., Loening-Baucke, V., Hale, L. P., & Lochs, H. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.7.3380-3389.2005 · Cited by 894 · cited 1× · see citing works
“host-disease after bone marrow transplantation [7], can further potentiate immunopathology by translocation via microlesions and ulcerations [5,8].”
BackgroundBacterial flagellin is a dominant antigen in Crohn disease
Lodes, M. J., Cong, Y., Elson, C. O., Mohamath, R., Landers, C. J., Targan, S. R., Fort, M., & Hershberg, R. M. (2004) · Journal of Clinical Investigation · doi:10.1172/jci200420295 · Cited by 802 · see citing works
Peripheral and Intestinal Regulatory CD4+CD25high T Cells in Inflammatory Bowel Disease
Maul, J., Loddenkemper, C., Mundt, P., Berg, E. G., Giese, T., Stallmach, A., Zeitz, M., & Duchmann, R. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.03.043 · Cited by 651 · see citing works
Self-citationCharacteristics of Intestinal Dendritic Cells in Inflammatory Bowel Diseases
Hart, A. L., Al-Hassi, H. O., Rigby, R. J., Bell, S., Emmanuel, A. V., Knight, S. C., Kamm, M. A., & Stagg, A. J. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.05.013 · Cited by 562 · see citing works
Fukata, M., Michelsen, K. S., Eri, R. D., Thomas, L. S., Hu, B., Lukasek, K., Nast, C. C., Lechago, J., Xu, R., Naiki, Y., et al. (2005) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00328.2004 · Cited by 508 · see citing works
Fukata, M., Chen, A., Klepper, A. L., Krishnareddy, S., Vamadevan, A. S., Thomas, L. S., Xu, R., Inoue, H., Arditi, M., Dannenberg, A. J., et al. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.06.017 · Cited by 456 · see citing works
Kim, S. C., Tonkonogy, S. L., Albright, C. A., Tsang, J., Balish, E., Braun, J., Huycke, M. M., & Sartor, R. B. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.02.009 · Cited by 433 · see citing works
Strategic Compartmentalization of Toll-Like Receptor 4 in the Mouse Gut
Ortega-Cava, C. F., Ishihara, S., Rumi, M. A. K., Kawashima, K., Ishimura, N., Kazumori, H., Udagawa, J., Kadowaki, Y., & Kinoshita, Y. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.8.3977 · Cited by 346 · see citing works
Heimesaat, M. M., Bereswill, S., Fischer, A., Fuchs, D., Struck, D., Niebergall, J., Jahn, H.-K., Dunay, I. R., Moter, A., Gescher, D. M., et al. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.12.8785 · Cited by 345 · see citing works
Self-citationRole of Toll-like Receptors in Spontaneous Commensal-Dependent Colitis
Rakoff-Nahoum, S., Hao, L., & Medzhitov, R. M. (2006) · Immunity · doi:10.1016/j.immuni.2006.06.010 · Cited by 343 · see citing works
Different Subsets of Enteric Bacteria Induce and Perpetuate Experimental Colitis in Rats and Mice
Rath, H. C., Schultz, M., Freitag, R., Dieleman, L. A., Li, F., Linde, H., Schölmerich, J., & Sartor, R. B. (2001) · Infection and Immunity · doi:10.1128/iai.69.4.2277-2285.2001 · Cited by 342 · see citing works
Beelen, D. W., Elmaagacli, A. H., Müller, K., Hirche, H., & Schaefer, U. W. (1999) · Blood · doi:10.1182/blood.v93.10.3267.410k22_3267_3275 · Cited by 270 · see citing works
MyD88-deficient mice develop severe intestinal inflammation in dextran sodium sulfate colitis
Araki, A., Kanai∥, T., Ishikura, T., Makita, S., Uraushihara, K., Iiyama, R., Totsuka, T., Takeda, K., Akira, S., & Watanabe, M. (2005) · Journal of Gastroenterology · doi:10.1007/s00535-004-1492-9 · Cited by 239 · see citing works
Waidmann, M., Bechtold, O., Frick, J.-S., Lehr, H.-A., Schubert, S., Dobrindt, U., Loeffler, J., Bohn, E., & Autenrieth, I. B. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)00672-3 · Cited by 234 · see citing works
Self-citationFort, M. M., Mozaffarian, A., Stöver, A. G., Correia, J. D. S., Johnson, D. A., Crane, R. T., Ulevitch, R. J., Persing, D. H., Bielefeldt-Ohmann, H., Probst, P., et al. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.10.6416 · Cited by 216 · see citing works
Mouse models for the study of Crohn's disease
Pizarro, T. T., Arseneau, K. O., Bamias, G., & Cominelli, F. (2003) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(03)00052-2 · Cited by 169 · see citing works
The Pathogenesis of Gastrointestinal Bacterial Overgrowth
Husebye, E. (2005) · Chemotherapy · doi:10.1159/000081988 · Cited by 168 · see citing works
Heimesaat, M. M., Fischer, A., Jahn, H.-K., Niebergall, J., Freudenberg, M. A., Blaut, M., Liesenfeld, O., Schumann, R. R., Göbel, U. B., & Bereswill, S. (2007) · Gut · doi:10.1136/gut.2006.104497 · Cited by 164 · see citing works
Self-citationHans, W., Schölmerich, J., Groß, V., & Falk, W. (2000) · European Journal of Gastroenterology & Hepatology · doi:10.1097/00042737-200012030-00002 · Cited by 145 · see citing works
Adenosine Kinase Inhibitor GP515 Improves Experimental Colitis in Mice
Siegmund, B., Rieder, F., Albrich, S. B., Wolf, K., Bidlingmaier, C., Firestein, G. S., Boyle, D., Lehr, H., Loher, F., Hartmann, G., et al. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)29668-3 · Cited by 128 · see citing works
Self-citationRuiz, P. A., Shkoda, A., Kim, S. C., Sartor, R. B., & Haller, D. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.5.2990 · Cited by 116 · see citing works
Involvement of Innate Immunity in the Development of Inflammatory and Autoimmune Diseases
Tlaskalová‐Hogenová, H., Tučková, L., Štëpánková, R., Hudcovic, T., Palová-Jelínková, L., Kozáková, H., Rossmann, P., Sánchez, D., Cinová, J., Hrnčíř, T., et al. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1361.122 · Cited by 80 · see citing works
CD40–CD40 Ligand Mediates the Recruitment of Leukocytes and Platelets in the Inflamed Murine Colon
Vowinkel, T., Anthoni, C., Wood, K. C., Stokes, K. Y., Russell, J., Gray, L. T., Bharwani, S., Senninger, N. J., Alexander, J. S., Krieglstein, C. F., et al. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.12.027 · Cited by 70 · see citing works
Vaccination preventsHelicobacter pylori-induced alterations of the gastric flora in mice
Aebischer, T., Fischer, A., Walduck, A. K., Schlötelburg, C., Lindig, M., Schreiber, S., Meyer, T. F., Bereswill, S., & Göbel, U. B. (2006) · FEMS Immunology & Medical Microbiology · doi:10.1111/rp10.1016-j.femsim.2004.05.008 · Cited by 64 · see citing works
Self-citationStevceva, L., Pavli, P., Buffinton, G. D., Wozniak, A., & Doe, W. F. (1999) · Journal of Gastroenterology and Hepatology · doi:10.1046/j.1440-1746.1999.01806.x · Cited by 47 · see citing works
The role of the Lps gene in experimental ulcerative colitis in mice
Lange, S., Delbro, D. S., Jennische, E., & Mattsby‐Baltzer, I. (1996) · Apmis · doi:10.1111/j.1699-0463.1996.tb04948.x · Cited by 46 · see citing works
Ruiz, P. A., Shkoda, A., Kim, S. C., Sartor, R. B., & Haller, D. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1326.023 · Cited by 45 · see citing works
Schuppler, M., Lötzsch, K., Waidmann, M., & Autenrieth, I. B. (2004) · Infection and Immunity · doi:10.1128/iai.72.4.1983-1990.2004 · Cited by 39 · see citing works
Inflammatory Bowel Disease: Is the Intestine a Trojan Horse?
Basset, C., & Holton, J. (2002) · Science Progress · doi:10.3184/003685002783238861 · Cited by 23 · see citing works
Siegmund, B., Rieder, F., Albrich, S. B., Firestein, G. S., Boyle, D., Hartmann, G., Endres, S., & Eigler, A. (2000) · Gastroenterology · doi:10.1016/s0016-5085(00)84448-0 · Cited by 8 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Microbial Influences in Inflammatory Bowel Diseases
Sartor, R. B. (2008) · Gastroenterology · doi:10.1053/j.gastro.2007.11.059 · Cited by 1,927 · see citing works
Host-Derived Nitrate Boosts Growth of <i>E. coli</i> in the Inflamed Gut
Winter, S. E., Winter, M. G., Xavier, M. N., Thiennimitr, P., Poon, V., Keestra, A. M., Laughlin, R. C., Gomez, G., Wu, J., Lawhon, S. D., et al. (2013) · Science · doi:10.1126/science.1232467 · Cited by 1,019 · see citing works
Dextran Sodium Sulphate Colitis Mouse Model: Traps and Tricks
Perše, M., & Cerar, A. (2012) · BioMed Research International · doi:10.1155/2012/718617 · Cited by 886 · see citing works
IL-33 is a crucial amplifier of innate rather than acquired immunity
Oboki, K., Ohno, T., Kajiwara, N., Arae, K., Morita, H., Ishii, A., Nambu, A., Abe, T., Kiyonari, H., Matsumoto, K., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1003059107 · Cited by 655 · see citing works
The role of microbiota in infectious disease
Stecher, B., & Hardt, W. (2008) · Trends in Microbiology · doi:10.1016/j.tim.2007.12.008 · Cited by 533 · see citing works
Microbial network disturbances in relapsing refractory Crohn’s disease
Swiss IBD Cohort Investigators, Yılmaz, B., Juillerat, P., Øyås, O., Ramon, C., Bravo, F. D., Franc, Y., Fournier, N., Michetti, P., Mueller, C., et al. (2019) · Nature Medicine · doi:10.1038/s41591-018-0308-z · Cited by 426 · see citing works
The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models
Nell, S., Suerbaum, S., & Josenhans, C. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2403 · Cited by 396 · see citing works
Berry, D., Schwab, C., Milinovich, G. J., Reichert, J., Mahfoudh, K. B., Decker, T., Engel, M., Hai, B., Hainzl, E., Heider, S., et al. (2012) · The ISME Journal · doi:10.1038/ismej.2012.39 · Cited by 333 · see citing works
Hayashi, A., Sato, T., Kamada, N., Mikami, Y., Matsuoka, K., Hisamatsu, T., Hibi∥, T., Roers, A., Yagita∥, H., Ohteki, T., et al. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.05.013 · Cited by 331 · see citing works
Bereswill, S., Muñoz, M., Fischer, A., Plickert, R., Haag, L.-M., Otto, B., Kühl, A. A., Loddenkemper, C., Göbel, U. B., & Heimesaat, M. M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015099 · Cited by 290 · see citing works
Self-citationFrosali, S., Pagliari, D., Gambassi, G., Landolfi, R., Pandolfi, F., & Cianci, R. (2015) · Journal of Immunology Research · doi:10.1155/2015/489821 · Cited by 278 · see citing works
Håkansson, Å., Tormo-Badia, N., Baridi, A., Xu, J., Molin, G., Hagslätt, M.-L. J., Karlsson, C., Jeppsson, B. W., Cilio, C., & Ahrné, S. (2014) · Clinical and Experimental Medicine · doi:10.1007/s10238-013-0270-5 · Cited by 263 · see citing works
The role of pattern recognition receptors in intestinal inflammation
Fukata, M., & Arditi, M. (2013) · Mucosal Immunology · doi:10.1038/mi.2013.13 · Cited by 255 · see citing works
Unveiling Colitis: A Journey through the Dextran Sodium Sulfate-induced Model
Yang, C., & Merlin, D. (2023) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izad312 · Cited by 253 · see citing works
Bereswill, S., Fischer, A., Plickert, R., Haag, L.-M., Otto, B., Kühl, A. A., Dasti, J. I., Zautner, A. E., Muñoz, M., Loddenkemper, C., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020953 · Cited by 245 · see citing works
Self-citationAcute dextran sulfate sodium (DSS)‐induced colitis promotes gut microbial dysbiosis in mice
Munyaka, P., Rabbi, M. F., Khafipour, E., & Ghia, J. (2016) · Journal of Basic Microbiology · doi:10.1002/jobm.201500726 · Cited by 226 · see citing works
Zhang, Q., Wu, Y., Wang, J., Wu, G. G., Long, W., Xue, Z., Wang, L., Zhang, X., Pang, X., Zhao, Y., et al. (2016) · Scientific Reports · doi:10.1038/srep27572 · Cited by 229 · see citing works
The importance of naming cryptic species and the conservation of endemic subterranean amphipods
Delić, T., Trontelj, P., Rendoš, M., & Fišer, C. (2017) · Scientific Reports · doi:10.1038/s41598-017-02938-z · Cited by 219 · see citing works
Heimesaat, M. M., Nogai, A., Bereswill, S., Plickert, R., Fischer, A., Loddenkemper, C., Steinhoff, U., Tchaptchet, S., Thiel, E., Freudenberg, M. A., et al. (2010) · Gut · doi:10.1136/gut.2009.197434 · Cited by 217 · see citing works
Self-citationUsing Corticosteroids to Reshape the Gut Microbiome: Implications for Inflammatory Bowel Diseases
Huang, E. Y., Inoue, T., Leone, V. A., Dalal, S., Touw, K., Wang, Y., Musch, M. W., Theriault, B., Higuchi, K., Donovan, S., et al. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000332 · Cited by 204 · see citing works
IL-33 and IL-33 Receptors in Host Defense and Diseases
Oboki, K., Ohno, T., Kajiwara, N., Saito, H., & Nakae, S. (2010) · Allergology International · doi:10.2332/allergolint.10-rai-0186 · Cited by 203 · see citing works
Nagalingam, N. A., Kao, J. Y., & Young, V. B. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21462 · Cited by 199 · see citing works
Interleukin-22 Induces Interleukin-18 Expression from Epithelial Cells during Intestinal Infection
Muñoz, M., Eidenschenk, C., Ota, N., Wong, K., Lohmann, U., Kühl, A. A., Wang, X., Manzanillo, P. S., Li, Y., Rutz, S., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.01.011 · Cited by 186 · see citing works
Self-citationRole of commensal gut bacteria in inflammatory bowel diseases
Loh, G., & Blaut, M. (2012) · Gut Microbes · doi:10.4161/gmic.22156 · Cited by 177 · see citing works
Self-citationPattern recognition receptors—Molecular orchestrators of inflammation in inflammatory bowel disease
Walsh, D. P., McCarthy, J., O’Driscoll, C. M., & Melgar, S. (2012) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2012.09.003 · Cited by 161 · see citing works
Yang, H., Wang, W., Romano, K. A., Gu, M., Sanidad, K. Z., Kim, D., Yang, J., Schmidt, B. A. R., Panigrahy, D., Pei, R., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aan4116 · Cited by 161 · see citing works
Graft-versus-host disease: regulation by microbe-associated molecules and innate immune receptors
Penack, O., Holler, E., & van den Brink, M. R. M. (2009) · Blood · doi:10.1182/blood-2009-09-242784 · Cited by 156 · see citing works
Immunotherapeutic mechanisms of anti-CD20 monoclonal antibodies
Taylor, R. P., & Lindorfer, M. A. (2008) · Current Opinion in Immunology · doi:10.1016/j.coi.2008.05.011 · Cited by 153 · see citing works
Kellermayer, R., Dowd, S. E., Harris, R. A., Balasa, A., Schaible, T. D., Wolcott, R. D., Tatevian, N., Szigeti, R. G., Li, Z., Versalovic, J. A., et al. (2011) · The FASEB Journal · doi:10.1096/fj.10-172205 · Cited by 145 · see citing works
Rausch, S., Held, J., Fischer, A., Heimesaat, M. M., Kühl, A. A., Bereswill, S., & Hartmann, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074026 · Cited by 142 · see citing works
Self-citationTranslating mouse vocalizations: prosody and frequency modulation1
Lahvis, G. P., Alleva, E., & Scattoni, M. L. (2010) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00603.x · Cited by 140 · see citing works
Ey, E., Torquet, N., Sourd, A. L., Leblond, C. S., Boeckers, T. M., Fauré, P., & Bourgeron, T. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.08.031 · Cited by 135 · see citing works
Ibrahim, A. A., Hugerth, L. W., Hases, L., Saxena, A., Seifert, M., Thomas, Q. A., Gustafsson, J.-Α., Engstrand, L. G., & Williams, C. (2018) · International Journal of Cancer · doi:10.1002/ijc.32037 · Cited by 139 · see citing works
Shang, L., Liu, H., Yu, H., Chen, M., Yang, T., Zeng, X., & Qiao, S. (2021) · Antibiotics · doi:10.3390/antibiotics10060643 · Cited by 137 · see citing works
Haag, L.-M., Fischer, A., Otto, B., Plickert, R., Kühl, A. A., Göbel, U. B., Bereswill, S., & Heimesaat, M. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035988 · Cited by 133 · see citing works
Self-citationHwang, D. H., Lee, H. J., Park, I. H., Seok, J. I., Kim, B. G., Joo, I. S., & Kim, S.-H. (2009) · Gene Therapy · doi:10.1038/gt.2009.80 · Cited by 132 · see citing works
Ng, S. C., Benjamin, J. L., McCarthy, N. E., Hedin, C. R. H., Koutsoumpas, A. L., Plamondon, S., Price, C. L., Hart, A. L., Kamm, M. A., Forbes, A., et al. (2010) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21590 · Cited by 122 · see citing works
Erridge, C., Duncan, S. H., Bereswill, S., & Heimesaat, M. M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009125 · Cited by 119 · see citing works
Self-citationThe Evolution of Meaning: Spatio-temporal Dynamics of Visual Object Recognition
Clarke, A., Taylor, K. I., & TYLER, L. K. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21544 · Cited by 118 · see citing works
Haag, L.-M., Fischer, A., Otto, B., Plickert, R., Kühl, A. A., Göbel, U. B., Bereswill, S., & Heimesaat, M. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040761 · Cited by 119 · see citing works
Self-citationIL-33 attenuates development and perpetuation of chronic intestinal inflammation
Gro, P., Doser, K., Falk, W., Obermeier, F., & Hofmann, C. (2012) · Inflammatory Bowel Diseases · doi:10.1002/ibd.22900 · Cited by 105 · see citing works
Toll-like receptors: promising therapeutic targets for inflammatory diseases
Achek, A., Yesudhas, D., & Choi, S. (2016) · Archives of Pharmacal Research · doi:10.1007/s12272-016-0806-9 · Cited by 102 · see citing works
Initial gut microbiota structure affects sensitivity to DSS-induced colitis in a mouse model
Li, M., Wu, Y., Hu, Y., Zhao, L., & Zhang, C.-H. (2017) · Science China Life Sciences · doi:10.1007/s11427-017-9097-0 · Cited by 3 · see citing works
Schicho, R., Nazyrova, A., Shaykhutdinov, R. A., Duggan, G. E., Vogel, H. J., & Storr, M. (2010) · Journal of Proteome Research · doi:10.1021/pr100547y · Cited by 96 · see citing works
Heimesaat, M. M., Boelke, S., Fischer, A., Haag, L.-M., Loddenkemper, C., Kühl, A. A., Göbel, U. B., & Bereswill, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040758 · Cited by 95 · see citing works
Self-citationDynamic Alteration of the Colonic Microbiota in Intestinal Ischemia-Reperfusion Injury
Wang, F., Li, Q., Wang, C., Tang, C. X., & Li, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042027 · Cited by 92 · see citing works
Toll-like receptor 4 (TLR4) antagonists as potential therapeutics for intestinal inflammation
Tam, J. S. Y., Coller, J. K., Hughes, P. A., Prestidge, C. A., & Bowen, J. M. (2021) · Indian Journal of Gastroenterology · doi:10.1007/s12664-020-01114-y · Cited by 91 · see citing works
Heimesaat, M. M., Fischer, A., Plickert, R., Wiedemann, T., Loddenkemper, C., Göbel, U. B., Bereswill, S., & Rieder, G. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100362 · Cited by 91 · see citing works
Self-citationPallav, K., Dowd, S. E., Villafuerte-Gálvez, J., Yang, X., Kabbani, T. A., Hansen, J., Dennis, M. D., Leffler, D. A., Newburg, D. S., & Kelly, C. P. (2014) · Gut Microbes · doi:10.4161/gmic.29558 · Cited by 85 · see citing works
Yue, B., Luo, X., Yu, Z., Mani, S., Wang, Z., & Dou, W. (2019) · Microorganisms · doi:10.3390/microorganisms7100440 · Cited by 86 · see citing works
Mesenteric fat—control site for bacterial translocation in colitis?
Batra, A., Heimesaat, M. M., Bereswill, S., Fischer, A., Glauben, R., Kunkel, D., Scheffold, A., Erben, U., Kühl, A. A., Loddenkemper, C., et al. (2012) · Mucosal Immunology · doi:10.1038/mi.2012.33 · Cited by 85 · see citing works
Self-citationLuo, H., Guo, P., & Zhou, Q. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046291 · Cited by 82 · see citing works
Space Environmental Factor Impacts upon Murine Colon Microbiota and Mucosal Homeostasis
Ritchie, L. E., Taddeo, S. S., Weeks, B. R., Lima, F., Bloomfield, S. A., Azcárate-Peril, M. A., Zwart, S. R., Smith, S. M., & Turner, N. D. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125792 · Cited by 80 · see citing works
Retinoic Acid Attenuates Ileitis by Restoring the Balance Between T-Helper 17 and T Regulatory Cells
Collins, C. B., Aherne, C. M., Kominsky, D. J., McNamee, E. N., Lebsack, M. D. P., Eltzschig, H. K., Jedlicka, P., & Rivera–Nieves, J. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.05.049 · Cited by 79 · see citing works
Ritchie, L. E., Sturino, J. M., Carroll, R. J., Rooney, L. W., Azcárate-Peril, M. A., & Turner, N. D. (2015) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiv008 · Cited by 78 · see citing works
Shaler, C. R., Parco, A. A., Elhenawy, W., Dourka, J., Jury, J., Verdu, E. F., & Coombes, B. K. (2021) · Nature Communications · doi:10.1038/s41467-021-26992-4 · Cited by 71 · see citing works
Holzscheiter, M., Layland, L. E., Loffredo‐Verde, E., Mair, K., Vogelmann, R., Langer, R., Wagner, H., & da Costa, C. P. (2013) · Clinical & Experimental Immunology · doi:10.1111/cei.12230 · Cited by 70 · see citing works
Collins, C. B., Aherne, C. M., McNamee, E. N., Lebsack, M. D. P., Eltzschig, H. K., Jedlicka, P., & Rivera–Nieves, J. (2011) · Gut · doi:10.1136/gutjnl-2011-300820 · Cited by 67 · see citing works
Tyagi, A., Kumar, U. P., Reddy, S., Santosh, V. S., Mohammed, S. B., Ehtesham, N. Z., & Ibrahim, A. (2012) · British Journal Of Nutrition · doi:10.1017/s0007114511007197 · Cited by 66 · see citing works
Ogawa, Y., Kawamura, T., Kimura, T., Ito, M., Blauvelt, A., & Shimada, S. (2009) · Blood · doi:10.1182/blood-2008-10-185728 · Cited by 66 · see citing works
Toll-like receptors as therapeutic targets in gastrointestinal diseases
Pimentel‐Nunes, P., Soares, J., Roncon‐Albuquerque, R., Dinis-Ribeiro, M. J., & Leite-Moreira, A. F. (2010) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728221003642027 · Cited by 66 · see citing works
Role of NF-κB activation in intestinal immune homeostasis
Wullaert, A. (2009) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2009.08.007 · Cited by 63 · see citing works
Ekmekçiu, I., von Klitzing, E., Fiebiger, U., Neumann, C., Bächer, P., Scheffold, A., Bereswill, S., & Heimesaat, M. M. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00167 · Cited by 61 · see citing works
Self-citationSharma, U., Olson, R., Erhart, F. N., Zhang, L., Meng, J., Segura, B. J., Banerjee, S., Sharma, M., Saluja, A. K., Ramakrishnan, S., et al. (2019) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjz188 · Cited by 60 · see citing works
Terán-Ventura, E., Aguilera, M., Vergara, P., & Martínez, V. (2014) · Journal of Crohn's and Colitis · doi:10.1016/j.crohns.2014.02.001 · Cited by 59 · see citing works
Hartmann, S., Schnoeller, C., Dahten, A., Avagyan, A., Rausch, S., Lendner, M., Bocian, C., Pillai, S., Loddenkemper, C., Lucius, R., et al. (2009) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2009.03290.x · Cited by 59 · see citing works
Self-citationMultifunctional role of dextran sulfate sodium for in vivo modeling of intestinal diseases
Rose, W., Sakamoto, K., & Leifer, C. A. (2012) · BMC Immunology · doi:10.1186/1471-2172-13-41 · Cited by 58 · see citing works
Schreiber, O., Petersson, J., Phillipson, M., Perry, M. A., Roos, S., & Holm, L. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90470.2008 · Cited by 58 · see citing works
Antigenic Modulation and Rituximab Resistance
Taylor, R. P., & Lindorfer, M. A. (2010) · Seminars in Hematology · doi:10.1053/j.seminhematol.2010.01.006 · Cited by 57 · see citing works
KHAN, I. A., Wei, J., Li, A., Liu, Z., Yang, P., Jing, Y., Chen, X., Zhao, T., Bai, Y., Zha, L., et al. (2022) · International Microbiology · doi:10.1007/s10123-022-00243-y · Cited by 56 · see citing works
Song, M., Kim, Y. J., Kim, Y.-H., Roh, J., Kim, S. U., & Yoon, B. (2010) · Human Gene Therapy · doi:10.1089/hum.2009.144 · Cited by 56 · see citing works
Keller, M., Ebstein, F., Bürger, E., Textoris‐Taube, K., Gorny, X., Urban, S., Zhao, F., Dannenberg, T., Sucker, A., Keller, C., et al. (2015) · European Journal of Immunology · doi:10.1002/eji.201445243 · Cited by 54 · see citing works
Toxoplasma gondii infection triggers chronic cachexia and sustained commensal dysbiosis in mice
Hatter, J. A., Kouche, Y. M., Melchor, S. J., Ng, K., Bouley, D. M., Boothroyd, J. C., & Ewald, S. E. (2018) · PLoS ONE · doi:10.1371/journal.pone.0204895 · Cited by 56 · see citing works
Tu, A., Wang, X. C., Chen, H., Jia, X., Wang, T., Yi, Y., Liu, B., Xin, W., Lü, X., & Shan, Y. (2021) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c00865 · Cited by 55 · see citing works
Haag, L.-M., Fischer, A., Otto, B., Grundmann, U., Kühl, A. A., Göbel, U. B., Bereswill, S., & Heimesaat, M. M. (2012) · European Journal of Microbiology and Immunology · doi:10.1556/eujmi.2.2012.1.2 · Cited by 54 · see citing works
Self-citationWohlgemuth, S., Haller, D., Blaut, M., & Loh, G. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.01883.x · Cited by 54 · see citing works
Self-citationRole of the Innate Immune System in the Pathogenesis of Inflammatory Bowel Disease
van Lierop, P. P. E., Samsom, J. N., Escher, J. C., & Nieuwenhuis, E. E. S. (2009) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e3181821964 · Cited by 53 · see citing works
Shi, Y., Gong, H., Zhao, Q., Liu, X., Liu, C., & Wang, H. (2019) · Toxicology Letters · doi:10.1016/j.toxlet.2019.08.012 · Cited by 52 · see citing works
Vitamin D Receptor Activation Improves Allergen-Triggered Eczema in Mice
Hartmann, B., Riedel, R., Jörß, K., Loddenkemper, C., Steinmeyer, A., Zügel, U., Babina, M., Radbruch, A., & Worm, M. (2011) · Journal of Investigative Dermatology · doi:10.1038/jid.2011.296 · Cited by 51 · see citing works
Self-citationvon Klitzing, E., Ekmekçiu, I., Bereswill, S., & Heimesaat, M. M. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.02590 · Cited by 49 · see citing works
Self-citationSeroprevalence of campylobacteriosis and relevant post-infectious sequelae
Zautner, A. E., Johann, C., Strubel, A., Busse, C., Tareen, A. M., Masanta, W. O., Lugert, R., Schmidt‐Ott, R., & Groß, U. (2014) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-2040-4 · Cited by 48 · see citing works
Samanta, A. K., Torok, V. A., Percy, N. J., Mashtoub, S., & Howarth, G. S. (2012) · The Journal of Microbiology · doi:10.1007/s12275-012-1362-8 · Cited by 49 · see citing works
Heimesaat, M. M., Dunay, I. R., Schulze, S., Fischer, A., Grundmann, U., Alutis, M. E., Kühl, A. A., Tamás, A., Tóth, G. K., Dunay, M. P., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108389 · Cited by 48 · see citing works
Self-citationGutiérrez‐Orozco, F., Thomas‐Ahner, J. M., Berman-Booty, L. D., Galley, J. D., Chitchumroonchokchai, C., Mace, T. A., Suksamrarn, S., Bailey, M. T., Clinton, S. K., Lesinski, G. B., et al. (2014) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201300771 · Cited by 48 · see citing works
Sannasiddappa, T. H., Costabile, A., Gibson, G. R., & Clarke, S. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023227 · Cited by 49 · see citing works
Olivier, S., Ilchmann-Diounou, H., Pochard, C., Frechin, L., Durieu, E., Foretz, M., Neunlist, M., Rolli‐Derkinderen, M., & Viollet, B. (2022) · Cells · doi:10.3390/cells11040590 · Cited by 45 · see citing works
Egan, C. E., Craven, M. D., Leng, J., Mack, M., Simpson, K. W., & Denkers, E. (2009) · Mucosal Immunology · doi:10.1038/mi.2009.105 · Cited by 45 · see citing works
Heimesaat, M. M., Giladi, E., Kühl, A. A., Bereswill, S., & Gozes, I. (2017) · Peptides · doi:10.1016/j.peptides.2017.12.023 · Cited by 45 · see citing works
Self-citationBereswill, S., Fischer, A., Plickert, R., Haag, L.-M., Otto, B., hl, A. A. K. ⁄., Dasti, J. I., Zautner, A. E., Muñoz, M., Loddenkemper, C., et al. (2011) · PLoS ONE · doi:10.1371/annotation/5247af81-4595-44b7-9c3f-2e45ad85abfa · Cited by 45 · see citing works
Self-citationReales‐Calderón, J. A., Vaz, C., Monteoliva, L., Molero, G., & Gil, C. (2016) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00605 · Cited by 44 · see citing works
Semin, I. K., Ninnemann, J., Bondareva, M. A., Gimaev, I., & Kruglov, A. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.644333 · Cited by 44 · see citing works
Li, Q., Zhang, Q., Wang, C., Tang, C., Zhang, Y., Li, N., & Li, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020460 · Cited by 43 · see citing works
How Gut Bacterial Dysbiosis Can Promote Candida albicans Overgrowth during Colonic Inflammation
Jawhara, S. (2022) · Microorganisms · doi:10.3390/microorganisms10051014 · Cited by 42 · see citing works
Bereswill, S., Plickert, R., Fischer, A., Kühl, A. A., Loddenkemper, C., Batra, A., Siegmund, B., Göbel, U. B., & Heimesaat, M. M. (2011) · European Journal of Microbiology and Immunology · doi:10.1556/eujmi.1.2011.3.8 · Cited by 42 · see citing works
Self-citationThöne‐Reineke, C., Fischer, A., Friese, C., Briesemeister, D., Göbel, U. B., Kammertoens, T., Bereswill, S., & Heimesaat, M. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113406 · Cited by 42 · see citing works
Self-citationNeutralization of pro‐inflammatory monocytes by targeting TLR2 dimerization ameliorates colitis
Shmuel-Galia, L., Aychek, T., Fink, A., Porat, Z., Zarmi, B., Bernshtein, B., Brenner, O. J., Jung, S., & Shai, Y. (2016) · The EMBO Journal · doi:10.15252/embj.201592649 · Cited by 41 · see citing works
Castro-Mejía, J. L., Jakesevic, M., Krych, Ł., Nielsen, D. S., Hansen, L. H., Sondergaard, B. C., Kvist, P. H., Hansen, A. K., & Holm, T. L. (2016) · Gastroenterology Research and Practice · doi:10.1155/2016/4953120 · Cited by 41 · see citing works
Inflammation in sporadic colorectal cancer.
Moossavi, S., & Bishehsari, F. (2012) · PubMed · Cited by 41 · see citing works
Cording, S., Fleissner, D., Heimesaat, M. M., Bereswill, S., Loddenkemper, C., Uematsu, S., Akira, S., Hamann, A., & Huehn, J. (2013) · European Journal of Microbiology and Immunology · doi:10.1556/eujmi.3.2013.1.1 · Cited by 40 · see citing works
Self-citationHasby, E. A., Saad, M. A. H., Shohieb, Z. S., & Noby, K. E. (2015) · Cellular Immunology · doi:10.1016/j.cellimm.2015.02.013 · Cited by 40 · see citing works
- Authors
- Heimesaat, M. M., Fischer, A., Siegmund, B., Kupz, A., Niebergall, J., Fuchs, D., Jahn, H.-K., Freudenberg, M., Loddenkemper, C., Batra, A., Lehr, H.-A., Liesenfeld, O., Blaut, M., Göbel, U. B., Schumann, R. R., & Bereswill, S.
- Affiliations
- Charité – Universitätsmedizin Berlin (DE)
- Max Planck Society (DE)
- Centre Hospitalier Universitaire Vaudois (CH)
- Corresponding author
- Bereswill, Stefan
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2007-07-25
- Volume
- 2
- Issue
- 7
- Pages
- e662
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC1914380
- OpenAlex
- W2065205410
- Cited by
- 213
- References
- 36
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 10 · 2022: 6 · 2021: 11 · 2020: 7 · 2019: 12 · 2018: 7 · 2017: 11 · 2016: 8 · 2015: 16 · 2014: 16 · 2013: 16 · 2012: 26
- FWCI
- 6.09
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- SERVAL (Université de Lausanne) (publishedVersion, other-oa)
- ResearchOnline - JCU (James Cook University) (submittedVersion)
- IRIS (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Sonnenfeld Stiftung
- Deutsche Forschungsgemeinschaft (KFO104, SFB633, Project 6, SPP1110)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- acute colitis, gut microbiota, TLR2, TLR4, Escherichia coli, DSS-induced colitis, Gram-negative bacteria, neutrophil recruitment, regulatory T cells, interferon-gamma, Bacteroides-Prevotella, Enterococcus, intestinal barrier injury, inflammatory bowel disease
- MeSH terms
- Acute Disease, Animals, Bacterial Infections, Colitis, Colon, Humans, Inflammation, Mice, Inbred C57BL, Neutrophils, Inflammatory Bowel Diseases, Signal Transduction, Toll-Like Receptor 2, Toll-Like Receptor 4, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
