The DOI matches its Crossref record; 47 of the 48 references it cites were found in a registry or an index.
Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response
Abstract
The immunomodulatory effect of probiotics has been shown mainly in gastro-intestinal immune disorders and little information is available on the inflammation of central nervous system. Recently we reported that IRT5 probiotics, a mixture of 5 probiotics, could suppress diverse experimental inflammatory disorders. In this study, we evaluated the prophylactic and therapeutic effects of IRT5 probiotics in experimental autoimmune encephalomyelitis (EAE), a T cell mediated inflammatory autoimmune disease of the central nervous system. Pretreatment of IRT5 probiotics before disease induction significantly suppressed EAE development. In addition, treatment with IRT5 probiotics to the ongoing EAE delayed the disease onset. Administration of IRT5 probiotics inhibited the pro-inflammatory Th1/Th17 polarization, while inducing IL10(+) producing or/and Foxp3(+) regulatory T cells, both in the peripheral immune system and at the site of inflammation. Collectively, our data suggest that IRT5 probiotics could be applicable to modulate T cell mediated neuronal autoimmune diseases, including multiple sclerosis.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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?
In the citing paper
“Animal studies suggest that probiotics can modulate endogenous neuroactive molecules [17], prevent and treat neuronal autoimmune diseases [18], and ameliorate impaired spatial memory in diabetic rats [19].”
From Effect of Supplementation with Probiotics in Patients with Schizophrenia: Systematic Review and Meta-Analysis of Randomized Controlled Clinical Trials (2025) · cites this paper as [18]
In the citing paper
“The supplementation of a cocktail of five probiotics (IRT5) before or after the EAE onset in rodents is associated with the delay of the disease onset or suppression of the disease progression, respectively (154).”
From The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology (2020) · cites this paper as [154]
In the citing paper
“The amelioration of the disease upon probiotic treatment was associated with a higher abundance of Treg cells, higher production of IL-10 by CD4+ T cells, B cells, and CD11c+ cells, together with the suppression of the pro-inflammatory Th-1/Th-17 response (154).”
From The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology (2020) · cites this paper as [154]
Citations
Cites
Vignali, D. A. A., Collison, L. W., & Workman, C. J. (2008) · Nature Reviews Immunology · doi:10.1038/nri2343 · Cited by 3,463
The regulation of IL-10 production by immune cells
Saraiva, M., & O’Garra, A. (2010) · Nature reviews. Immunology · doi:10.1038/nri2711 · Cited by 3,293
Steinman, R. M., Hawiger, D., & Nussenzweig, M. C. (2003) · Annual Review of Immunology · doi:10.1146/annurev.immunol.21.120601.141040 · Cited by 3,162
Immunology of multiple sclerosis
Sospedra, M., & Martin, R. (2005) · Annual Review of Immunology · doi:10.1146/annurev.immunol.23.021704.115707 · Cited by 2,149
A function for interleukin 2 in Foxp3-expressing regulatory T cells
Fontenot, J. D., Rasmussen, J. P., Gavin, M. A., & Rudensky, A. Y. (2005) · Nature Immunology · doi:10.1038/ni1263 · Cited by 1,819
Interactions between commensal intestinal bacteria and the immune system
Macpherson, A. J., & Harris, N. L. (2004) · Nature reviews. Immunology · doi:10.1038/nri1373 · Cited by 1,683
Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis
Lee, Y. K., Menezes, J. S., Umesaki, Y., & Mazmanian, S. K. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000082107 · Cited by 1,323
Gut immune maturation depends on colonization with a host-specific microbiota
Chung, H., Pamp, S. J., Hill, J. A., Surana, N. K., Edelman, S. M., Troy, E. B., Reading, N. C., Villablanca, E. J., Wang, S., Mora, J. R., et al. (2012) · Cell · doi:10.1016/j.cell.2012.04.037 · Cited by 1,241
Chaudhry, A., Samstein, R. M., Treuting, P., Liang, Y., Pils, M. C., Heinrich, J.-M., Jack, R. S., Wunderlich, F. T., Brüning, J. C., Müller, W., et al. (2011) · Immunity · doi:10.1016/j.immuni.2011.03.018 · Cited by 980
T cells in multiple sclerosis and experimental autoimmune encephalomyelitis
Fletcher, J. M., Lalor, S. J., Sweeney, C. M., Tubridy, N. J., & Mills, K. H. G. (2010) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2010.04143.x · Cited by 975
O’Connor, R. A., Prendergast, C. T., Sabatos, C. A., Lau, C. W. Z., Leech, M. D., Wraith, D. C., & Anderton, S. M. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.6.3750 · Cited by 945
Interleukin-10 Therapy—Review of a New Approach
Asadullah, K., Sterry, W., & Volk, H. (2003) · Pharmacological Reviews · doi:10.1124/pr.55.2.4 · Cited by 941
Probiotics and the gut microbiota in intestinal health and disease
Gareau, M. G., Sherman, P. M., & Walker, W. A. (2010) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2010.117 · Cited by 907
Smits, H. H., Engering, A. J., van der Kleij, D., de Jong, E. C., Schipper, K., van Capel, T. M. M., Zaat, B. A. J., Yazdanbakhsh, M., Wierenga, E. A., & van Kooyk, Y. (2005) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2005.03.036 · Cited by 778
The immune system and the gut microbiota: friends or foes?
Cerf-Bensussan, N., & Gaboriau-Routhiau, V. (2010) · Nature Reviews Immunology · doi:10.1038/nri2850 · Cited by 704
Differential regulation of central nervous system autoimmunity by TH1 and TH17 cells
Stromnes, I. M., Cerretti, L., Liggitt, D., Harris, R. A., & Goverman, J. M. (2008) · Nature Medicine · doi:10.1038/nm1715 · Cited by 644
Kwon, H., Lee, C., So, J., Chae, C.-S., Hwang, J.-S., Sahoo, A., Nam, J. H., Rhee, J. H., Hwang, K.-C., & Im, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904055107 · Cited by 642
Huber, S., Gagliani, N., Esplugues, E., O'Connor, W., Huber, F. J., Chaudhry, A., Kamanaka, M., Kobayashi, Y., Booth, C. J., Rudensky, A. Y., et al. (2011) · Immunity · doi:10.1016/j.immuni.2011.01.020 · Cited by 602
New concepts in the immunopathogenesis of multiple sclerosis
Hemmer, B., Archelos, J. J., & Hartung, H. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn784 · Cited by 598
Role of Gut Commensal Microflora in the Development of Experimental Autoimmune Encephalomyelitis
Ochoa-Repáraz, J., Mielcarz, D. W., Ditrio, L. E., Burroughs, A. R., Foureau, D. M., Haque-Begum, S., & Kasper, L. H. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900747 · Cited by 590
Bettelli, E., Das, M. P., Howard, E. D., Weiner, H. L., Sobel, R. A., & Kuchroo, V. K. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.7.3299 · Cited by 560
Giacinto, C. D., Marinaro, M., Sanchez, M., Strober, W., & Boirivant, M. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.6.3237 · Cited by 522
Glucocorticoids upregulate FOXP3 expression and regulatory T cells in asthma
Karagiannidis, C., Akdiş, M., Holopainen, P., Woolley, N., Hense, G., Rückert, B., Mantel, P., Menz, G., Akdiş, C. A., Blaser, K., et al. (2004) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2004.07.014 · Cited by 516
McCarthy, J., O’Mahony, L., O’Callaghan, L., Sheil, B., Vaughan, E. E., Fitzsimons, N., Fitzgibbon, J., O’Sullivan, G. C., Kiely, B., Collins, J. K., et al. (2003) · Gut · doi:10.1136/gut.52.7.975 · Cited by 462
Calcinaro, F., Dionisi, S., Marinaro, M., Candeloro, P., Bonato, V., Marzotti, S., Corneli, R. B., Ferretti, E., Gulino, A., Grasso, F., et al. (2005) · Diabetologia · doi:10.1007/s00125-005-1831-2 · Cited by 364
Siffrin, V., Radbruch, H., Glumm, R., Niesner, R., Paterka, M., Herz, J., Leuenberger, T., Lehmann, S. M., Luenstedt, S., Rinnenthal, J. L., et al. (2010) · Immunity · doi:10.1016/j.immuni.2010.08.018 · Cited by 325
Current Views on the Roles of Th1 and Th17 Cells in Experimental Autoimmune Encephalomyelitis
Behi, M. E., Rostami, A. M., & Ćirić, B. (2010) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-009-9188-9 · Cited by 222
Revival of CD8+ Treg–mediated suppression
Smith, T. R. F., & Kumar, V. (2008) · Trends in Immunology · doi:10.1016/j.it.2008.04.002 · Cited by 199
Sheil, B., McCarthy, J., O’Mahony, L., Bennett, M. W., Ryan, P., Fitzgibbon, J. J., Kiely, B., Collins, J. K., & Shanahan, F. (2004) · Gut · doi:10.1136/gut.2003.027789 · Cited by 187
Regulatory B cells in autoimmunity: developments and controversies
Mauri, C., & Blair, P. (2010) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2010.140 · Cited by 181
Ueno, N., Fujiya, M., Segawa, S., Nata, T., Moriichi, K., Tanabe, H., Mizukami, Y., Kobayashi, N., Ito, K., & Kohgo, Y. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21597 · Cited by 130
Regulatory T cells in the central nervous system
Lowther, D. E., & Hafler, D. A. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01130.x · Cited by 128
So, J., Song, M., Kwon, H., Lee, C., Chae, C.-S., Sahoo, A., Jash, A., Lee, S. H., Park, Z., & Im, S. (2010) · Life Sciences · doi:10.1016/j.lfs.2010.12.013 · Cited by 122
Furrie, E. (2005) · Proceedings of The Nutrition Society · doi:10.1079/pns2005466 · Cited by 108
Bhasin, M., Wu, M., & Tsirka, S. (1997) · BMC Immunology · doi:10.1186/1471-2172-8-10 · Cited by 95
Lactobacillus casei potentiates induction of oral tolerance in experimental arthritis
So, J., Lee, C., Kwon, H., Yi, H., Chae, C.-S., Park, J.-N., Hwang, K., & Im, S. (2008) · Molecular Immunology · doi:10.1016/j.molimm.2008.07.038 · Cited by 89
Nguyen, X. D., & Robinson, D. S. (2004) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2004.04.048 · Cited by 87
Sheil, B., MacSharry, J. A., O'Callaghan, L., O'Riordan, A., Waters, A., Morgan, J. G., Collins, J. K., O’Mahony, L., & Shanahan, F. (2006) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2006.03051.x · Cited by 70
Microbiota and Autoimmune Disease: The Hosted Self
Mathis, D. J., & Benoist, C. O. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.09.007 · Cited by 66
Immunosuppressive Drugs and Tregs
Serres, S. A. D., Sayegh, M. H., & Najafian, N. (2009) · Clinical Journal of the American Society of Nephrology · doi:10.2215/cjn.03180509 · Cited by 66
Health, Probiotics, and Inflammation
Mengheri, E. (2008) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0b013e31817eedc4 · Cited by 59
Prophylactic Effect of Probiotics on the Development of Experimental Autoimmune Myasthenia Gravis
Chae, C.-S., Kwon, H., Hwang, J., Kim, J., & Im, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052119 · Cited by 54
Kobayashi, T., Suzuki, T., Kaji, R., Serata, M., Nagata, T., Ando, M., Iizuka, R., Tsujibe, S., Murakami, J., Kiyoshima‐Shibata, J., et al. (2011) · Immunopharmacology and Immunotoxicology · doi:10.3109/08923973.2010.617755 · Cited by 41
Kobayashi, T., Kato, I., Nanno, M., Shida, K., Shibuya, K., Matsuoka, Y., & Onoue, M. (2009) · Immunopharmacology and Immunotoxicology · doi:10.3109/08923970903200716 · Cited by 38
NIETHAMMER, D., Kümmerle-Deschner, J. B., & Dannecker, G. E. (1999) · Lara D. Veeken · doi:10.1093/rheumatology/38.8.747 · Cited by 34
Bar‐Or, A., Oger, J., Gibbs, E., Niino, M., Aziz, T., Renoux, C., Alatab, S., Shi, F., Campagnolo, D. I., Jalili, F., et al. (2009) · Multiple Sclerosis Journal · doi:10.1177/1352458509106230 · Cited by 13
The TH17 kiss of death for neurons
Leavy, O. (2010) · Nature reviews. Immunology · doi:10.1038/nri2876 · Cited by 3
Research works printed but not linked: 2
- Ochoa-Reparaz, 2009, Role of gut commensal microflora in the development of experimental autoimmune encephalomyelitis, J. Immunol., 183, 6041, 10.4049/jimmunol.0900747 · DOI · Paper page
- Smits, 2005, Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin, J. Allergy Clin. Immunol., 115, 1260, 10.1016/j.jaci.2005.03.036 · DOI
Cited by
Sorted by citations
The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology
Rutsch, A., Kantsjö, J. B., & Ronchi, F. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.604179 · Cited by 821
The role of microbiome in central nervous system disorders
Wang, Y., & Kasper, L. H. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.12.015 · Cited by 803
“The role of microbiom dx.doi.org/10.1016/j.bbi.2013.12.015 strains of Bifidobacterium genus, tend to alleviate murine EAE symptoms via reciprocal regulation of pro- and anti-inflammatory cytokine responses (Kobayashi et al., 2010, 2012; Kwon et al., 2013; Lavasani et al., 2010).”
InfluentialPropionic Acid Shapes the Multiple Sclerosis Disease Course by an Immunomodulatory Mechanism
Duscha, A., Gisevius, B., Hirschberg, S., Yissachar, N., Stangl, G. I., Dawin, E., Bader, V., Haase, S., Kaisler, J., David, C., et al. (2020) · Cell · doi:10.1016/j.cell.2020.02.035 · Cited by 654
Microbiome, probiotics and neurodegenerative diseases: deciphering the gut brain axis
Westfall, S., Lomis, N., Kahouli, I., Dia, S. Y., Singh, S. P., & Prakash, S. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2550-9 · Cited by 570
“Induced IL-10 and/or Foxp3(?) regulatory T cells [158]”
BackgroundAutism Spectrum Disorders and the Gut Microbiota
Fattorusso, A., Di Genova, L., Dell’Isola, G., Mencaroni, E., & Esposito, S. (2019) · Nutrients · doi:10.3390/nu11030521 · Cited by 484
“In addition, GF and CF diets only reduce levels of two toxins, gluteomorphins and caseomorphins but cannot heal the mucosa or restore gut microbiota composition [150].”
Background
Metadata
- Authors
- Kwon, H.-K., Kim, G.-C., Kim, Y., Hwang, W., Jash, A., Sahoo, A., Kim, J.-E., Nam, J. H., & Im, S.-H.
- Affiliations
- Harvard University (US)
- Gwangju Institute of Science and Technology (KR)
- Chonnam National University (KR)
- Washington University in St. Louis (US)
- Corresponding author
- Im, Sin-Hyeog
- ORCID
- Venue
- Clinical Immunology
- Publisher
- Elsevier BV
- Published
- 2013-03
- Volume
- 146
- Issue
- 3
- Pages
- 217-227
- ISSN
- 1521-6616 (ISSN-L)
- OpenAlex
- W2078792455
- Cited by
- 212
- References
- 48
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 11 · 2023: 29 · 2022: 20 · 2021: 27 · 2020: 19 · 2019: 20 · 2018: 23 · 2017: 24 · 2016: 12 · 2015: 11 · 2014: 2 · 2013: 2
- FWCI
- 6.62
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Clinical Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Research Foundation (2011-0028529)
- Systems Biology Infrastructure Establishment Grant
- Topics
- Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- experimental autoimmune encephalomyelitis, probiotics, T helper cell polarization, Th1/Th17 cells, regulatory T cells, Foxp3, IL-10, immunomodulation, multiple sclerosis, neuroinflammation, T cell-mediated autoimmunity
- MeSH terms
- Animals, Encephalomyelitis, Autoimmune, Experimental, T-Lymphocytes, Helper-Inducer, Mice, Inbred C57BL, Peptide Fragments, Spinal Cord, T-Lymphocyte Subsets, Probiotics, Mice, Myelin-Oligodendrocyte Glycoprotein
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