Desulfovibrio vulgaris caused gut inflammation and aggravated DSS-induced colitis in C57BL/6 mice model.
Desulfovibrio vulgaris
Colitis
Gut microbiota
Short-chain fatty acid
Sulfate-reducing bacteria
Journal
Gut pathogens
ISSN: 1757-4749
Titre abrégé: Gut Pathog
Pays: England
ID NLM: 101474263
Informations de publication
Date de publication:
26 Jul 2024
26 Jul 2024
Historique:
received:
04
06
2024
accepted:
10
07
2024
medline:
27
7
2024
pubmed:
27
7
2024
entrez:
26
7
2024
Statut:
epublish
Résumé
Sulfate-reducing bacteria (SRB) is a potential pathogen usually detected in patients with gastrointestinal diseases. Hydrogen sulfide (H2S), a metabolic byproduct of SRB, was considered the main causative agent that disrupted the morphology and function of gut epithelial cells. Associated study also showed that flagellin from Desulfovibrio vulgaris (DVF), the representative bacterium of the Desulfovibrio genus, could exacerbate colitis due to the interaction of DVF and LRRC19, leading to the secretion of pro-inflammatory cytokines. However, we still have limited understanding about the change of gut microbiota (GM) composition caused by overgrowth of SRB and its exacerbating effects on colitis. In this study, we transplanted D. vulgaris into the mice treated with or without DSS, and set a one-week recovery period to investigate the impact of D. vulgaris on the mice model. The outcomes showed that transplanted D. vulgaris into the normal mice could cause the gut inflammation, disrupt gut barrier and reduce the level of short-chain fatty acids (SCFAs). Moreover, D. vulgaris also significantly augmented DSS-induced colitis by exacerbating the damage of gut barrier and the secretion of inflammatory cytokines, for instance, IL-1β, iNOS, and TNF-α. Furthermore, results also showed that D. vulgaris could markedly change GM composition, especially decrease the relative abundance of SCFAs-producing bacteria. Additionally, D. vulgaris significantly stimulated the growth of Akkermansia muciniphila probably via its metabolic byproduct, H2S, in vivo. Collectively, this study indicated that transplantation of D. vulgaris could cause gut inflammation and aggravate the colitis induced by DSS.
Sections du résumé
BACKGROUND
BACKGROUND
Sulfate-reducing bacteria (SRB) is a potential pathogen usually detected in patients with gastrointestinal diseases. Hydrogen sulfide (H2S), a metabolic byproduct of SRB, was considered the main causative agent that disrupted the morphology and function of gut epithelial cells. Associated study also showed that flagellin from Desulfovibrio vulgaris (DVF), the representative bacterium of the Desulfovibrio genus, could exacerbate colitis due to the interaction of DVF and LRRC19, leading to the secretion of pro-inflammatory cytokines. However, we still have limited understanding about the change of gut microbiota (GM) composition caused by overgrowth of SRB and its exacerbating effects on colitis.
RESULTS
RESULTS
In this study, we transplanted D. vulgaris into the mice treated with or without DSS, and set a one-week recovery period to investigate the impact of D. vulgaris on the mice model. The outcomes showed that transplanted D. vulgaris into the normal mice could cause the gut inflammation, disrupt gut barrier and reduce the level of short-chain fatty acids (SCFAs). Moreover, D. vulgaris also significantly augmented DSS-induced colitis by exacerbating the damage of gut barrier and the secretion of inflammatory cytokines, for instance, IL-1β, iNOS, and TNF-α. Furthermore, results also showed that D. vulgaris could markedly change GM composition, especially decrease the relative abundance of SCFAs-producing bacteria. Additionally, D. vulgaris significantly stimulated the growth of Akkermansia muciniphila probably via its metabolic byproduct, H2S, in vivo.
CONCLUSIONS
CONCLUSIONS
Collectively, this study indicated that transplantation of D. vulgaris could cause gut inflammation and aggravate the colitis induced by DSS.
Identifiants
pubmed: 39060944
doi: 10.1186/s13099-024-00632-w
pii: 10.1186/s13099-024-00632-w
doi:
Types de publication
Journal Article
Langues
eng
Pagination
39Subventions
Organisme : National Nature Science Foundation of China
ID : 31900103 & 31900498
Organisme : National Nature Science Foundation of China
ID : 31900103 & 31900498
Informations de copyright
© 2024. The Author(s).
Références
Zhai L, Huang C, Ning Z, Zhang Y, Zhuang M, Yang W, et al. Ruminococcus gnavus plays a pathogenic role in diarrhea-predominant irritable bowel syndrome by increasing serotonin biosynthesis. Cell Host Microbe. 2023;31:33–e445.
doi: 10.1016/j.chom.2022.11.006
pubmed: 36495868
Long Y, Tang L, Zhou Y, Zhao S, Zhu H. Causal relationship between gut microbiota and cancers: a two-sample mendelian randomisation study. BMC Med. 2023;21:66.
doi: 10.1186/s12916-023-02761-6
pubmed: 36810112
pmcid: 9945666
Newman KL, Kamada N. Pathogenic associations between oral and gastrointestinal diseases. Trends Mol Med. 2022;28:1030–9.
doi: 10.1016/j.molmed.2022.05.006
pubmed: 35691866
pmcid: 9691515
Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev. 2012;92.
Figliuolo VR, Dos Santos LM, Abalo A, Nanini H, Santos A, Brittes NM, et al. Sulfate-reducing bacteria stimulate gut immune responses and contribute to inflammation in experimental colitis. Life Sci. 2017;189:29–38.
doi: 10.1016/j.lfs.2017.09.014
pubmed: 28912045
Li G, Liu H, Yu Y, Wang Q, Yang C, Yan Y et al. Desulfovibrio desulfuricans and its derived metabolites confer resistance to FOLFOX through METTL3. eBioMedicine. 2024;102.
Singh SB, Carroll-Portillo A, Lin HC. Desulfovibrio Gut: Enemy within? Microorganisms. 2023;11:1772.
pubmed: 37512944
Khan I, Huang G, Li X, Liao W, Leong WK, Xia W, et al. Mushroom polysaccharides and jiaogulan saponins exert cancer preventive effects by shaping the gut microbiota and microenvironment in apc mice. Pharmacol Res. 2019;148:104448.
doi: 10.1016/j.phrs.2019.104448
pubmed: 31499195
Xia W, Khan I, Li X, Huang G, Yu Z, Leong WK, et al. Adaptogenic flower buds exert cancer preventive effects by enhancing the SCFA-producers, strengthening the epithelial tight junction complex and immune responses. Pharmacol Res. 2020;159:104809.
doi: 10.1016/j.phrs.2020.104809
pubmed: 32502642
Ijssennagger N, van der Meer R, van Mil SWC. Sulfide as a mucus barrier-breaker in inflammatory bowel disease? Trends Mol Med. 2016;22:190–9.
doi: 10.1016/j.molmed.2016.01.002
pubmed: 26852376
Oh G-S, Pae H-O, Lee B-S, Kim B-N, Kim J-M, Kim H-R, et al. Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kappab via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic Biol Med. 2006;41:106–19.
doi: 10.1016/j.freeradbiomed.2006.03.021
pubmed: 16781459
Kushkevych I, Dordević D, Vítězová M. Possible synergy effect of hydrogen sulfide and acetate produced by sulfate-reducing bacteria on inflammatory bowel disease development. J Adv Res. 2021;27:71–8.
doi: 10.1016/j.jare.2020.03.007
pubmed: 33318867
Rowan F, Docherty NG, Murphy M, Murphy TB, Coffey JC, O’Connell PR. Bacterial colonization of colonic crypt mucous gel and disease activity in ulcerative colitis. Ann Surg. 2010;252:869–75.
doi: 10.1097/SLA.0b013e3181fdc54c
pubmed: 21037444
Huang G, Su L, Zhang N, Han R, Leong WK, Li X et al. The prebiotic and anti-fatigue effects of hyaluronan. Front Nutr. 2022;12.
An Y, Zhai Z, Wang X, Ding Y, He L, Li L et al. Targeting Desulfovibrio vulgaris flagellin-induced NAIP/NLRC4 inflammasome activation in macrophages attenuates ulcerative colitis. J Adv Res. 2023;S2090123223002242.
Schmitt M, Schewe M, Sacchetti A, Feijtel D, van de Geer WS, Teeuwssen M, et al. Paneth cells respond to inflammation and contribute to tissue regeneration by acquiring stem-like features through SCF/c-Kit signaling. Cell Rep. 2018;24:2312–e23287.
doi: 10.1016/j.celrep.2018.07.085
pubmed: 30157426
Huang M, Su J, Lou Z, Xie F, Pan W, Yang Z, et al. Application of a DSS colitis model in toxicologically assessing norisoboldine. Toxicol Mech Methods. 2020;30:107–14.
doi: 10.1080/15376516.2019.1669242
pubmed: 31532267
Bian X, Li N, Tan B, Sun B, Guo M-Q, Huang G, et al. Polarity-tuning Derivatization-LC-MS Approach for probing global carboxyl-containing metabolites in Colorectal Cancer. Anal Chem. 2018;90:11210–5.
doi: 10.1021/acs.analchem.8b01873
pubmed: 30193063
Huang G, Khan I, Li X, Chen L, Leong W, Ho LT, et al. Ginsenosides Rb3 and rd reduce polyps formation while reinstate the dysbiotic gut microbiota and the intestinal microenvironment in ApcMin/+ mice. Sci Rep. 2017;7:12552.
doi: 10.1038/s41598-017-12644-5
pubmed: 28970547
pmcid: 5624945
Corano Scheri K, Hsieh Y-W, Jeong E, Fawzi AA. Limited Hyperoxia-Induced proliferative retinopathy (LHIPR) as a model of Retinal Fibrosis, Angiogenesis, and inflammation. Cells. 2023;12:2468.
doi: 10.3390/cells12202468
pubmed: 37887312
pmcid: 10605514
Fritsch SD, Sukhbaatar N, Gonzales K, Sahu A, Tran L, Vogel A et al. Metabolic support by macrophages sustains colonic epithelial homeostasis. Cell Metabol. 2023;S1550413123003418.
Weglarz L, Dzierzewicz Z, Skop B, Orchel A, Parfiniewicz B, Wiśniowska B, et al. Desulfovibrio desulfuricans lipopolysaccharides induce endothelial cell IL-6 and IL-8 secretion and E-selectin and VCAM-1 expression. Cell Mol Biol Lett. 2003;8:991–1003.
pubmed: 14668922
Dzierzewicz Z, Szczerba J, Lodowska J, Wolny D, Gruchlik A, Orchel A, et al. The role of Desulfovibrio desulfuricans lipopolysaccharides in modulation of periodontal inflammation through stimulation of human gingival fibroblasts. Arch Oral Biol. 2010;55:515–22.
doi: 10.1016/j.archoralbio.2010.05.001
pubmed: 20593542
Nie Y, Xie X-Q, Zhou L, Guan Q, Ren Y, Mao Y, et al. Desulfovibrio fairfieldensis-derived outer membrane vesicles damage epithelial barrier and induce inflammation and Pyroptosis in macrophages. Cells. 2022;12:89.
doi: 10.3390/cells12010089
pubmed: 36611884
pmcid: 9818291
Parada Venegas D, De la Fuente MK, Landskron G, González MJ, Quera R, Dijkstra G, et al. Short chain fatty acids (SCFAs)-Mediated gut epithelial and Immune Regulation and its relevance for inflammatory Bowel diseases. Front Immunol. 2019;10:277.
doi: 10.3389/fimmu.2019.00277
pubmed: 30915065
pmcid: 6421268
He J, Zhang P, Shen L, Niu L, Tan Y, Chen L, et al. Short-chain fatty acids and their association with signalling pathways in inflammation, glucose and lipid metabolism. Int J Mol Sci. 2020;21:6356.
doi: 10.3390/ijms21176356
pubmed: 32887215
pmcid: 7503625
Yang W, Yu T, Huang X, Bilotta AJ, Xu L, Lu Y, et al. Intestinal microbiota-derived short-chain fatty acids regulation of immune cell IL-22 production and gut immunity. Nat Commun. 2020;11:4457.
doi: 10.1038/s41467-020-18262-6
pubmed: 32901017
pmcid: 7478978
Tang Y, Pingitore F, Mukhopadhyay A, Phan R, Hazen TC, Keasling JD. Pathway confirmation and flux analysis of central metabolic pathways in Desulfovibrio vulgaris hildenborough using gas chromatography-mass spectrometry and Fourier transform-ion cyclotron resonance mass spectrometry. J Bacteriol. 2007;189:940–9.
doi: 10.1128/JB.00948-06
pubmed: 17114264
Cani PD, Depommier C, Derrien M, Everard A, de Vos WM. Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms. Nat Rev Gastroenterol Hepatol. 2022.
Hänninen A, Toivonen R, Pöysti S, Belzer C, Plovier H, Ouwerkerk JP, et al. Akkermansia muciniphila induces gut microbiota remodelling and controls islet autoimmunity in NOD mice. Gut. 2018;67:1445–53.
doi: 10.1136/gutjnl-2017-314508
pubmed: 29269438
Depommier C, Everard A, Druart C, Plovier H, Van Hul M, Vieira-Silva S, et al. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study. Nat Med. 2019;25:1096–103.
doi: 10.1038/s41591-019-0495-2
pubmed: 31263284
pmcid: 6699990
Zhang T, Ji X, Lu G, Zhang F. The potential of Akkermansia muciniphila in inflammatory bowel disease. Appl Microbiol Biotechnol. 2021;105:5785–94.
doi: 10.1007/s00253-021-11453-1
pubmed: 34312713
Hill-Burns EM, Debelius JW, Morton JT, Wissemann WT, Lewis MR, Wallen ZD, et al. Parkinson’s disease and Parkinson’s disease medications have distinct signatures of the gut microbiome. Mov Disord. 2017;32:739–49.
doi: 10.1002/mds.26942
pubmed: 28195358
pmcid: 5469442