New probiotic strains for inflammatory bowel disease management identified by combining in vitro and in vivo approaches
Open accessAbstract
Alterations in the gut microbiota composition play a key role in the development of chronic diseases such as inflammatory bowel disease (IBD). The potential use of probiotics therefore gained attention, although outcomes were sometimes conflicting and results largely strain-dependent. The present study aimed to identify new probiotic strains that have a high potential for the management of this type of pathologies. Strains were selected from a large collection by combining different in vitro and in vivo approaches, addressing both anti-inflammatory potential and ability to improve the gut barrier function. We identified six strains with an interesting anti-inflammatory profile on peripheral blood mononuclear cells and with the ability to restore the gut barrier using a gut permeability model based on Caco-2 cells sensitized with hydrogen peroxide. The in vivo evaluation in two 2,4,6-trinitrobenzene sulfonic acid-induced murine models of colitis highlighted that some of the strains exhibited beneficial activities against acute colitis while others improved chronic colitis. Bifidobacterium bifidum PI22, the strain that exhibited the most protective capacities against acute colitis was only slightly efficacious against chronic colitis, while Bifidobacterium lactis LA804 which was less efficacious in the acute model was the most protective against chronic colitis. Lactobacillus helveticus PI5 was not anti-inflammatory in vitro but the best in strengthening the epithelial barrier and as such able to significantly dampen murine acute colitis. Interestingly, Lactobacillus salivarius LA307 protected mice significantly against both types of colitis. This work provides crucial clues for selecting the best strains for more efficacious therapeutic approaches in the management of chronic inflammatory diseases. The strategy employed allowed us to identify four strains with different characteristics and a high potential for the management of inflammatory diseases, such as IBD.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Animal studies have found that Bifidobacterium P122, Lactobacillus LA804, and Lactobacillus Switzerland are beneficial in colitis.
“Animal studies have found that Bifidobacterium P122, Lactobacillus LA804, and Lactobacillus Switzerland are beneficial in colitis (138).”
From Stress triggers flare of inflammatory bowel disease in children and adults (2019) · cites this paper as [138]
Cites
Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease
Hugot, J.-P., Chamaillard, M., Zouali, H., Lesage, S., Cézard, J.-P., Belaiche, J., Almer, S., Tysk, C., O'Morain, C. A., Gassull, M., et al. (2001) · Nature · doi:10.1038/35079107 · Cited by 5,591 · see citing works
Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermúdez-Humarán, L. G., Gratadoux, J.-J., Blugeon, S., Bridonneau, C., Furet, J.-P., Corthier, G., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804812105 · Cited by 4,413 · see citing works
Self-citationReduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach
Manichanh, C., Rigottier-Gois, L., Bonnaud, E., Gloux, K., Pelletier, E., Frangeul, L., Nalin, R., Jarrin, C., Chardon, P., Marteau, P., et al. (2006) · Gut · doi:10.1136/gut.2005.073817 · Cited by 2,277 · see citing works
Hampe, J., Franke, A., Rosenstiel, P. C., Till, A., Teuber, M., Huse, K., Albrecht, M., Gabriele Mayr, B., Vega, F. M. D. L., Briggs, J. C., et al. (2006) · Nature Genetics · doi:10.1038/ng1954 · Cited by 1,899 · see citing works
Unravelling the effects of the environment and host genotype on the gut microbiome
Spor, A., Koren, O., & Ley, R. (2011) · Nature Reviews Microbiology · doi:10.1038/nrmicro2540 · Cited by 1,509 · 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
Sartor, R. B. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.03.024 · Cited by 1,053 · see citing works
Michielan, A., & D’Incà, R. (2015) · Mediators of Inflammation · doi:10.1155/2015/628157 · Cited by 709 · see citing works
Course of ulcerative colitis: Analysis of changes in disease activity over years
Langholz, E., Munkholm, P., Davidsen, M., & Binder, V. (1994) · Gastroenterology · doi:10.1016/0016-5085(94)90054-x · Cited by 689 · see citing works
Deletion polymorphism upstream of IRGM associated with altered IRGM expression and Crohn's disease
McCarroll, S. A., Huett, A., Kuballa, P., Chilewski, S. D., Landry, A., Goyette, P., Zody, M. C., Hall, J. L., Brant, S. R., Cho, J. H., et al. (2008) · Nature Genetics · doi:10.1038/ng.215 · Cited by 655 · see citing works
Chantret, I., Rodolosse, A., Barbat, A., Dussaulx, E., Brot‐Laroche, E., Zweibaum, A., & Rousset, M. (1994) · Journal of Cell Science · doi:10.1242/jcs.107.1.213 · Cited by 447 · see citing works
Wallace, J. L., MacNaughton, W. K., Morris, G. P., & Beck, P. L. (1989) · Gastroenterology · doi:10.1016/0016-5085(89)90760-9 · Cited by 435 · see citing works
Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria
Foligné, B. (2007) · World Journal of Gastroenterology · doi:10.3748/wjg.v13.i2.236 · Cited by 432 · see citing works
Seth, A., Yan, F., Polk, D. B., & Rao, R. K. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00202.2007 · Cited by 404 · see citing works
Sáez‐Lara, M. J., Gómez‐Llorente, C., Plaza‐Díaz, J., & Gil, Á. (2015) · BioMed Research International · doi:10.1155/2015/505878 · Cited by 390 · see citing works
Fernandez, E. M., Valenti, V., Rockel, C., Hermann, C., Pot, B., Boneca, I. G., & Grangette, C. (2011) · Gut · doi:10.1136/gut.2010.232918 · Cited by 376 · see citing works
Vivinus-Nébot, M., Frin-Mathy, G., Bzioueche, H., Dainese, R., Bernard, G., Anty, R., Filippi, J., Saint‐Paul, M., Tulić, M. K., Verhasselt, V., et al. (2013) · Gut · doi:10.1136/gutjnl-2012-304066 · Cited by 365 · see citing works
Dupont, A. W., Richards, Jelinek, K. A., Krill, J. T., Rahimi, E. F., & Ghouri, Y. A. (2014) · Clinical and Experimental Gastroenterology · doi:10.2147/ceg.s27530 · Cited by 303 · see citing works
A Key Role of Dendritic Cells in Probiotic Functionality
Foligné, B., Ζουμποπούλου, Γ., Dewulf, J., Younes‐Chennoufi, A. B., Chareyre, F., Sirard, J., Pot, B., & Grangette, C. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000313 · Cited by 278 · see citing works
Self-citationAmeho, C. K., Adjei, A. A., Harrison, E., Takeshita, K., Morioka, T., Arakaki, Y., Ito, E., Suzuki, I., Kulkarni, A. D., Kawajiri, A., et al. (1997) · Gut · doi:10.1136/gut.41.4.487 · Cited by 234 · see citing works
Prosberg, M. V., Bendtsen, F., Vind, I., Petersen, A. M., & Gluud, L. L. (2016) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365521.2016.1216587 · Cited by 210 · see citing works
Probiotics in the management of irritable bowel syndrome and inflammatory bowel disease
Whelan, K., & Quigley, E. M. M. (2013) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e32835d7bba · Cited by 185 · see citing works
Barbara, G., Zecchi, L., Barbaro, M. R., Cremon, C., Bellacosa, L., Marcellini, M. M., GIORGIO, R. D., Corinaldesi, R., & Stanghellini, V. (2012) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e318264e918 · Cited by 79 · see citing works
Martín, R., Laval, L., Chain, F., Miquel, S., Natividad, J. M., Cherbuy, C., Sokol, H., Verdu, E. F., Vlieg, J. V. H., Bermúdez‐Humarán, L. G., et al. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00608 · Cited by 78 · see citing works
Paneth Cell Alterations in the Development and Phenotype of Crohn’s Disease
Stappenbeck, T. S., & McGovern, D. P. B. (2016) · Gastroenterology · doi:10.1053/j.gastro.2016.10.003 · Cited by 56 · see citing works
Burns, P., Alard, J., Hrdý, J., Boutillier, D., Páez, R., Reinheimer, J. A., Pot, B., Vinderola, G., & Grangette, C. (2017) · Scientific Reports · doi:10.1038/srep43211 · Cited by 48 · see citing works
Self-citationMachtaler, S., Knieling, F., Luong, R. H., Tian, L., & Willmann, J. K. (2015) · Theranostics · doi:10.7150/thno.13048 · Cited by 46 · see citing works
Neau, E., Delannoy, J., Marion, C., Cottart, C., Labellie, C., Holowacz, S., Butel, M., Kapel, N., & Waligora‐Dupriet, A. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.03440-15 · Cited by 43 · see citing works
Self-citationCellular and Molecular Mechanisms in the Two Major Forms of Inflammatory Bowel Disease
Bene, L., Falus, A., Baffy, N. J., & Fulop, A. K. (2011) · Pathology & Oncology Research · doi:10.1007/s12253-011-9397-4 · Cited by 28 · see citing works
Residual inflammation and ulcerative colitis in remission.
Moss, A. C. (2014) · PubMed · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Lactobacillus spp. for Gastrointestinal Health: Current and Future Perspectives
Dempsey, E., & Corr, S. C. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.840245 · Cited by 579 · see citing works
Stress triggers flare of inflammatory bowel disease in children and adults
Sun, Y., Li, L., Xie, R., Wang, B., Jiang, K., & Cao, H. (2019) · Frontiers in Pediatrics · doi:10.3389/fped.2019.00432 · Cited by 171 · see citing works
- Authors
- Alard, J., Peucelle, V., Boutillier, D., Breton, J., Kuylle, S., Pot, B., Holowacz, S., & Grangette, C.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- GENIBIO, Le Pradas, ZI du Couserans, 09190 Lorp-Sentaraille, France.
- PiLeJe (France) (FR)
- Venue
- Beneficial Microbes
- Publisher
- Walter de Gruyter GmbH
- Published
- 2018-02-27
- Volume
- 9
- Issue
- 2
- Pages
- 317-332
- ISSN
- 1876-2883 (ISSN-L)
- 1876-2891
- OpenAlex
- W2791085365
- Cited by
- 78
- References
- 30
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 8 · 2023: 9 · 2022: 13 · 2021: 14 · 2020: 7 · 2019: 10 · 2018: 8
- FWCI
- 9.15
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Beneficial Microbes (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- VUBIR (Vrije Universiteit Brussel) (submittedVersion)
- Funders
- Institut National de la Santé et de la Recherche Médicale
- Centre National de la Recherche Scientifique
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- probiotic strains, inflammatory bowel disease, colitis, anti-inflammatory activity, intestinal barrier, intestinal permeability, Bifidobacterium bifidum, Bifidobacterium animalis subsp. lactis, Lactobacillus helveticus, Lactobacillus salivarius, 2,4,6-trinitrobenzene sulfonic acid, Caco-2 cells, peripheral blood mononuclear cells, strain selection
- MeSH terms
- Animals, Anti-Inflammatory Agents, Bifidobacterium, Cells, Cultured, Colitis, Disease Models, Animal, Humans, Hydrogen Peroxide, Intestinal Mucosa, Lactobacillus, Mice, Inbred BALB C, Permeability, Trinitrobenzenesulfonic Acid, Inflammatory Bowel Diseases, Cytokines, Caco-2 Cells, Probiotics, Mice, Immunomodulation
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
