Volume 10, Issue 3 (9-2022)                   JoMMID 2022, 10(3): 122-128 | Back to browse issues page

XML Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Salimi A, Rohani M, Pourshafie M R. Investigating the Relation between the Gut Microbiota and Inflammatory Bowel Disease in a Mouse Model. JoMMID 2022; 10 (3) :122-128
URL: http://jommid.pasteur.ac.ir/article-1-476-en.html
Investigating the Relation between the Gut Microbiota and Inflammatory Bowel Disease in a Mouse Model
Afsaneh Salimi , Mahdi Rohani , Mohammad Reza Pourshafie
Department of Bacteriology, Pasteur Institute of Iran, Tehran, Iran
Abstract:   (845 Views)
Introduction: Inflammatory bowel disease (IBD) is a group of chronic gastrointestinal disorders affecting millions worldwide. Several factors are involved in developing this disease, but gut microbiota is known to be one of the most critical factors. This study investigated the relationship between gut microbiota and IBD in a mouse model. Methods: In this study, two methods were used: chemical induction with dextran sulfate sodium (DSS) and biological induction with stool from a human with IBD (fecal microbiota transplantation) to induce inflammation in the gut of mice. The gut microbiota populations in both groups were studied using real-time PCR. In addition, the serum levels of inflammatory cytokines and the colon tissues of the mice were analyzed. Results: The pathological results showed that the colon tissue in the FMT group had inflammatory changes as in the DSS group. The changes in the gut microbiota population in both FMT and DSS groups on the last day of the study also showed a similar pattern. Interleukin-1 and IL-6 also increased in the FMT and DSS groups compared to the control group. Conclusion: Our results showed a mutual relationship between gut microbiota and inflammatory diseases and that gut microbiota was not only the cause of IBD but may also be a consequence of this disease. In fact, by chemically inducing inflammation, the gut microbiota was altered. On the other hand, performing FMT from human stool with IBD altered the gut microbiota of mice and induced inflammatory disease in the mouse model.
Keywords: Inflammatory bowel disease, Gut microbiota, Fecal microbiota transplantation, Dextran sulfate sodium
Full-Text [PDF 905 kb]   (390 Downloads)    
Type of Study: Original article | Subject: Microbial pathogenesis
Received: 2022/06/13 | Accepted: 2022/09/19 | Published: 2022/10/12
References
1. O'Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006; 7 (7): 688-93. [DOI:10.1038/sj.embor.7400731]
2. Wrzosek L, Ciocan D, Borentain P, Spatz M, Puchois V, Hugot C, et al. Transplantation of human microbiota into conventional mice durably reshapes the gut microbiota. Sci Rep. 2018; 6854. [DOI:10.1038/s41598-018-25300-3]
3. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008; 134 (2): 577-94. [DOI:10.1053/j.gastro.2007.11.059]
4. Seyedian SS, Nokhostin F, Malamir MD. A review of the diagnosis, prevention, and treatment methods of inflammatory bowel disease. J Med Life. 2019; 12 (2): 113-22.
5. Kaser A, Zeissig S, Blumberg RS. Inflammatory bowel disease. Annu Rev Immunol. 2010; 28: 573-621. [DOI:10.1146/annurev-immunol-030409-101225]
6. Baumgart DC, Sandborn WJ. Crohn's disease. Lancet. 2012; 380 (9853): 1590-605. [DOI:10.1016/S0140-6736(12)60026-9]
7. Ordas I, Eckmann L, Talamini M, Baumgart DC, Sandborn WJ. Ulcerative colitis. Lancet. 2012; 380 (9853): 1606-19. [DOI:10.1016/S0140-6736(12)60150-0]
8. Bjerrum JT, Wang Y, Hao F, Coskun M, Ludwiget CH, et al. Metabonomics of human fecal extracts characterize ulcerative colitis, Crohn's disease, and healthy individuals. Metabolomics. 2015; 11: 122-33. [DOI:10.1007/s11306-014-0677-3]
9. Ananthakrishnan AN. Epidemiology and risk factors for IBD. Nature reviews. Nat Rev Gastroenterol Hepatol. 2015; 12 (4): 205-17. [DOI:10.1038/nrgastro.2015.34]
10. Casen C, Veb HC, Sekelja M, Hegge FT, Karlsson MK, et al. Deviations in human gut microbiota: a novel diagnostic test for determining dysbiosis in patients with IBS or IBD. Aliment Pharmacol Ther. 2015; 42 (1): 71-83. [DOI:10.1111/apt.13236]
11. Frank DN, Robertson CE, Hamm CM, Kpadeh Z, Zhang T, et al. Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2011; 17 (1): 179-84. [DOI:10.1002/ibd.21339]
12. Walker AW, Sanderson JD, Churcher C, Parkes GC, et al. High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease. BMC Microbiol. 2011; 11: 7. [DOI:10.1186/1471-2180-11-7]
13. Gevers D, Kugathasan S, Denson LA, Vázquez-Baeza Y, Treuren WV, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe. 2014; 15 (3): 382-92. [DOI:10.1016/j.chom.2014.02.005]
14. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, et al. A human gut microbial gene catalog established by metagenomic sequencing. Nature. 2010; 464 (7285): 59-65. [DOI:10.1038/nature08821]
15. Arumugam M, Raes J, Pelletier E, Paslier DL, et al. Enterotypes of the human gut microbiome. Nature. 2011; 473 (7346): 174-80. [DOI:10.1038/nature09944]
16. Schloissnig S, Arumugam M, Sunagawa S, Mitreva M, et al. Genomic variation landscape of the human gut microbiome. Nature. 2013; 493 (7430): 45-50. [DOI:10.1038/nature11711]
17. Arrieta MC, Walter J, Finlay BB. Human Microbiota-Associated Mice: A Model with Challenges. Cell Host Microbe. 2016; 19 (5): 575-78. [DOI:10.1016/j.chom.2016.04.014]
18. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, and Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 2009; 1 (6): 6-14. [DOI:10.1126/scitranslmed.3000322]
19. Han Y, Zhao T, Cheng X, Zhao M, Gong SH, et al. Cortical Inflammation is Increased in a DSS-Induced Colitis Mouse Model. Neurosci Bull. 2018; 34 (6): 1058-66. [DOI:10.1007/s12264-018-0288-5]
20. Bartosch S, Fite A, Macfarlane G, McMurdo ME. Characterization of Bacterial Communities in Feces from Healthy Elderly Volunteers and Hospitalized Elderly Patients by Using Real-Time PCR and Effects of Antibiotic Treatment on the Fecal Microbiota. Appl Environ Microbiol. 2004; 70 (6): 3575-81. [DOI:10.1128/AEM.70.6.3575-3581.2004]
21. Haarman M, Knol J. Quantitative Real-Time PCR Analysis of Fecal Lactobacillus Species in Infants Receiving a Prebiotic Infant Formula. Appl Environ Microbiol. 2006; 72 (40: 2359-65. [DOI:10.1128/AEM.72.4.2359-2365.2006]
22. Jia W, Whitehead R. N, Griffiths L, Dawson C, Waring R. H, Ramsden DB, et al. Is the abundance of Faecalibacterium prausnitzii relevant to Crohn's disease? FEMS Microbiol Lett. 2010; 310 (2): 138-44. [DOI:10.1111/j.1574-6968.2010.02057.x]
23. De Gregoris TB, Aldred N, Clare AS, Burgess JG. Improvement of phylum- and class-specific primers for real-time PCR quantification of bacterial taxa. J Microbiol Methods. 2011; 86 (3): 351-56. [DOI:10.1016/j.mimet.2011.06.010]
24. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods. 2001; 25 (4): 402-8. [DOI:10.1006/meth.2001.1262]
25. Tlaskalová-Hogenová H, Štˇepánková R, Kozáková H, Hudcovic T, Vannucci L, et al. 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. 2011; 8 (2): 110-20. [DOI:10.1038/cmi.2010.67]
26. Homann C, Dollive S, Grunberg S, Chen J, Li H, et al. Archaea and fungi of the human gut microbiome: Correlations with diet and bacterial residents. PLoS ONE. 2013; 8 (6): e66019. [DOI:10.1371/journal.pone.0066019]
27. Frank DN, Amand ALS., Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA. 2007; 104 (34): 13780-85. [DOI:10.1073/pnas.0706625104]
28. Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: An integrative view. Cell. 2012; 148 (6): 1258-70. [DOI:10.1016/j.cell.2012.01.035]
29. Rosen CE, Palm NW. Navigating the Microbiota Seas: Triangulation Finds a Way Forward. Cell Host Microbe. 2018; 23 (1): 1-3. [DOI:10.1016/j.chom.2017.12.015]
30. Gkouskou K, Deligianni C, Tsatsanis C, Eliopoulos AG. The gut microbiota in mouse models of inflammatory bowel disease. Front Cell Infect Microbiol. 2014; 4: 28. [DOI:10.3389/fcimb.2014.00028]
31. Licht TR, Madsen B, Wilcks A. Selection of bacteria originating from a human intestinal microbiota in the gut of previously germ-free rats. FEMS Microbiol Lett. 2007; 277 (2): 205-9. [DOI:10.1111/j.1574-6968.2007.00962.x]
32. Hirayama K, Itoh K, Takahashi E, Mitsuoka T. Comparison of composition of fecal microbiota and metabolism of fecal bacteria among human flora- associated mice inoculated with feces from 6 different human donors. Microb Ecol Health Dis. 1995; 8 (5):199-211. https://doi.org/10.1002/(SICI)1234-987X(199609)9:5<199::AID-MEH428>3.3.CO;2-S [DOI:10.1002/(SICI)1234-987X(199609)9:53.3.CO;2-S]
33. Tomas J, Wrzosek L, Bouznad N, Bouet S, Mayeur C, Noordine ML, et al. Primocolonization is associated with colonic epithelial maturation during conventionalization. FASEB J. 2013; 27 (2): 645-55. [DOI:10.1096/fj.12-216861]
34. Chung H, Pamp SJ, Hill JA, Surana NK, Edelman SM, Troy EB, et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell. 2012; 149 (7): 1578-93. [DOI:10.1016/j.cell.2012.04.037]
35. Gaboriau-Routhiau V, Rakotobe S, Lécuyer E, Mulder I, Lan A, Bridonneau C, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity. 2009; 31 (4): 677-89. [DOI:10.1016/j.immuni.2009.08.020]
36. Macpherson AJ, Harris NL. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol. 2004; 4 (6): 478-85. [DOI:10.1038/nri1373]
37. Morgun A, Dzutsev A, Dong X, Greer RL, Sexton DJ, Ravel J, et al. Uncovering effects of antibiotics on the host and microbiota using transkingdom gene networks. Gut. 2015; 64 (11): 1732-43. [DOI:10.1136/gutjnl-2014-308820]
38. Wlodarska M, Willing B, Keeney KM, Menendez A, Bergstrom KS, Gill N, et al. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect Immun. 2011; 79 (4): 1536-45. [DOI:10.1128/IAI.01104-10]
39. Wei Y-L, Chen Y-Q, Gong H, Li N, Wu K-Q, Hu W, et al. Fecal Microbiota Transplantation Ameliorates Experimentally Induced Colitis in Mice by Upregulating AhR. Front Microbiol. 2018; 9: 1921. [DOI:10.3389/fmicb.2018.01921]
40. Pavel FM, Vesa CM, Gheorghe G, Diaconu CC, Stoicescu M, et al. Highlighting the Relevance of Gut Microbiota Manipulation in Inflammatory Bowel Disease. Diagnostics. 2021; 11 (6): 1090. [DOI:10.3390/diagnostics11061090]
41. Peterson DA, Frank DN, Pace NR, Gordon JI. Metagenomic approaches for defining the pathogenesis of inflammatory bowel diseases. Cell Host Microbe. 2008; 3 (6): 417-27. [DOI:10.1016/j.chom.2008.05.001]
42. Fujimoto T, Imaeda H, Takahashi K, Kasumi E, Bamba S, Fukiyama Y, et al. Decreased abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn's disease. J Gastroenterol Hepatol. 2013; 28 (4): 609-13. [DOI:10.1111/jgh.12073]
43. Baldelli V, Scaldaferri F, Putignani L, Chierico FD. The Role of Enterobacteriaceae in Gut Microbiota Dysbiosis in Inflammatory Bowel Diseases. Microorganisms. 2021; 9 (4): 697. [DOI:10.3390/microorganisms9040697]
44. Wu Z, Pan D, Jiang M, Sang L, Chang B. Selenium-Enriched Lactobacillus acidophilus Ameliorates Dextran Sulfate Sodium-Induced Chronic Colitis in Mice by Regulating Inflammatory Cytokines and Intestinal Microbiota. Front Med. 2021; 8: 716816. [DOI:10.3389/fmed.2021.716816]
Add your comments about this article : Your username or Email:
CAPTCHA
Send email to the article author

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.