Human-derived probiotic Lactobacillus reuteri strains differentially reduce intestinal inflammation
Open accessAbstract
Lactobacillus reuteri (L. reuteri) is a probiotic that inhibits the severity of enteric infections and modulates the immune system. Human-derived L. reuteri strains DSM17938, ATCC PTA4659, ATCC PTA 5289, and ATCC PTA 6475 have demonstrated strain-specific immunomodulation in cultured monocytoid cells, but information about how these strains affect inflammation in intestinal epithelium is limited. We determined the effects of the four different L. reuteri strains on lipopolysaccharide (LPS)-induced inflammation in small intestinal epithelial cells and in the ileum of newborn rats. IPEC-J2 cells (derived from the jejunal epithelium of a neonatal piglet) and IEC-6 cells (derived from the rat crypt) were treated with L. reuteri. Newborn rat pups were gavaged cow milk formula supplemented with L. reuteri strains in the presence or absence of LPS. Protein and mRNA levels of cytokines and histological changes were measured. We demonstrate that even though one L. reuteri strain (DSM 17938) did not inhibit LPS-induced IL-8 production in cultured intestinal cells, all strains significantly reduced intestinal mucosal levels of KC/GRO (∼IL-8) and IFN-γ when newborn rat pups were fed formula containing LPS ± L. reuteri. Intestinal histological damage produced by LPS plus cow milk formula was also significantly reduced by all four strains. Cow milk formula feeding (without LPS) produced mild gut inflammation, evidenced by elevated mucosal IFN-γ and IL-13 levels, a process that could be suppressed by strain 17938. Other cytokines and chemokines were variably affected by the different strains, and there was no toxic effect of L. reuteri on intestinal cells or mucosa. In conclusion, L. reuteri strains differentially modulate LPS-induced inflammation. Probiotic interactions with both epithelial and nonepithelial cells in vivo must be instrumental in modulating intrinsic anti-inflammatory effects in the intestine. We suggest that the terms anti- and proinflammatory be used only to describe the effects of a probiotic in the living host.
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Mice administered Lactobacillus reuteri demonstrate improvements in GI and behavioral manifestations.
“Mice administered Lactobacillus reuteri demonstrate improvements in GI and behavioral manifestations [90, 91].”
From Serotonin as a link between the gut-brain-microbiome axis in autism spectrum disorders (2018) · cites this paper as [91]
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Lactobacillus species prevents colitis in interleukin 10 gene–deficient mice
Madsen, K. L., Doyle, J. S. G., Jewell, L. D., Tavernini, M. M., & Fedorak, R. N. (1999) · Gastroenterology · doi:10.1016/s0016-5085(99)70013-2 · Cited by 761 · see citing works
Cario, E., Rosenberg, I. M., Brandwein, S. L., Beck, P. L., Reinecker, H., & Podolsky, D. K. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.2.966 · Cited by 751 · see citing works
Abreu, M. T., Vora, P., Faure, E., Thomas, L. S., Arnold, E. T., & Arditi, M. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.3.1609 · Cited by 681 · see citing works
Epithelial cells as sensors for microbial infection.
Kagnoff, M. F., & Eckmann, L. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119522 · Cited by 619 · see citing works
Mechanisms of action of probiotics: Recent advances
Ng, S. C., Hart, A. L., Kamm, M. A., Stagg, A. J., & Knight, S. C. (2009) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20602 · Cited by 596 · see citing works
Otte, J., Cario, E., & Podolsky, D. K. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.01.007 · Cited by 506 · see citing works
Abrahamsson, T., Jakobsson, T., Böttcher, M. F., Fredrikson, M. G., Jenmalm, M. C., Björkstén, B., & Oldæus, G. (2007) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2007.01.007 · Cited by 476 · see citing works
Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors
Jones, S. E., & Versalovic, J. A. (2009) · BMC Microbiology · doi:10.1186/1471-2180-9-35 · Cited by 417 · see citing works
The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession.
Reuter, G. (2001) · PubMed · Cited by 417 · see citing works
Schierack, P., Nordhoff, M., Pollmann, M., Weyrauch, K. D., Amasheh, S., Lodemann, U., Jores, J., Babila, J. T., Kleta, S., Blikslager, A. T., et al. (2005) · Histochemistry and Cell Biology · doi:10.1007/s00418-005-0067-z · Cited by 379 · see citing works
Commensal-Induced Regulatory T Cells Mediate Protection against Pathogen-Stimulated NF-κB Activation
O’Mahony, C., Scully, P., O'Mahony, D., Murphy, S., O'Brien, F., Lyons, A., Sherlock, G., MacSharry, J. A., Kiely, B., Shanahan, F., et al. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000112 · Cited by 365 · see citing works
Valeur, N., Engel, P. A., Carbajal, N., Connolly, E., & Ladefoged, K. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.2.1176-1181.2004 · Cited by 343 · see citing works
Chemical characterization of an antimicrobial substance produced by Lactobacillus reuteri
Talarico, T. L., & Dobrogosz, W. J. (1989) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.33.5.674 · Cited by 314 · see citing works
Savino, F., Pelle, E., Palumeri, E., Oggero, R., & MINIERO, R. (2007) · PEDIATRICS · doi:10.1542/peds.2006-1222 · Cited by 303 · see citing works
Ma, D., Forsythe, P., & Bienenstock, J. (2004) · Infection and Immunity · doi:10.1128/iai.72.9.5308-5314.2004 · Cited by 289 · see citing works
Understanding the Susceptibility of the Premature Infant to Necrotizing Enterocolitis (NEC)
Hunter, C. J., Upperman, J. S., Ford, H. R., & Niklas, V. (2008) · Pediatric Research · doi:10.1203/pdr.0b013e31815ed64c · Cited by 246 · see citing works
Probiotic Lactobacillus reuteri suppress proinflammatory cytokines via c-Jun
Lin, Y. P., Thibodeaux, C., Peña, J. A., Ferry, G. D., & Versalovic, J. A. (2008) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20448 · Cited by 235 · see citing works
Lyons, A., O'Mahony, D., O'Brien, F., MacSharry, J. A., Sheil, B., Ceddia, M. A., Russell, W. M., Forsythe, P., Bienenstock, J., Kiely, B., et al. (2010) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2009.03437.x · Cited by 233 · see citing works
Nadler, E. P., Dickinson, E. C., Knisely, A. S., Zhang, X.-R., Boyle, P., Beer–Stolz, D., Watkins, S. C., & Ford, H. R. (2000) · Journal of Surgical Research · doi:10.1006/jsre.2000.5877 · Cited by 227 · see citing works
Suzuki, M., Hisamatsu, T., & Podolsky, D. K. (2003) · Infection and Immunity · doi:10.1128/iai.71.6.3503-3511.2003 · Cited by 217 · see citing works
Cytokine responses during mucosal infections: role in disease pathogenesis and host defence
Svanborg, C., Godaly, G., & Hedlund, M. (1999) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(99)80017-4 · Cited by 203 · see citing works
Haynes, T. E., Li, P., Li, X., Shimotori, K., Sato, H., Flynn, N. E., Wang, J., Knabe, D. A., & Wu, G. (2009) · Amino Acids · doi:10.1007/s00726-009-0243-x · Cited by 183 · see citing works
Probiotics and infectious diarrhea
Saavedra, J. M. (2000) · The American Journal of Gastroenterology · doi:10.1016/s0002-9270(99)00811-4 · Cited by 131 · see citing works
Mills, P. R. (2005) · Environmental Health · doi:10.1186/1476-069x-4-1 · Cited by 116 · see citing works
Feng, J., El-Assal, O. N., & Besner, G. E. (2006) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2005.10.018 · Cited by 111 · see citing works
Liu, Y., Zhu, L., Fatheree, N. Y., Liu, X., Pacheco, S. E., Tatevian, N., & Rhoads, J. M. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00182.2009 · Cited by 98 · see citing works
Self-citationTubelius, P., Stan, V., & Zachrisson, A. (2005) · Environmental Health · doi:10.1186/1476-069x-4-25 · Cited by 96 · see citing works
Peña, J. A., Li, S. Y., Wilson, P. H., Thibodeau, S. A., Szary, A. J., & Versalovic, J. A. (2004) · Applied and Environmental Microbiology · doi:10.1128/aem.70.1.558-568.2004 · Cited by 91 · see citing works
Probiotics in the United States
Vanderhoof, J. A., & Young, R. (2008) · Clinical Infectious Diseases · doi:10.1086/523339 · Cited by 88 · see citing works
Clinical Evidence for Immunomodulatory Effects of Probiotic Bacteria
Ruemmele, F. M., Bier, D. M., Marteau, P. R., Rechkemmer, G., Bourdet‐Sicard, R., Walker, W., & Goulet, O. (2009) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e31817d80ca · Cited by 82 · see citing works
Lactobacillus reuteri Tablets Suppress Helicobacter pylori Infection
Imase, K., Tanaka, A., Tokunaga, K., Sugano, H., Ishida, H., & Takahashi, S. (2007) · Kansenshogaku zasshi · doi:10.11150/kansenshogakuzasshi1970.81.387 · Cited by 65 · see citing works
Glutamine decreases lipopolysaccharide-induced intestinal inflammation in infant rats
Li, N., Liboni, K., Fang, M.-Z., Samuelson, D. A., Lewis, P., Patel, R., & Neu, J. (2004) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00493.2003 · Cited by 61 · see citing works
Zhang, L., Li, N., Robert, C. D., Fang, M.-Z., Liboni, K., McMahon, R., Caicedo, R. A., & Neu, J. (2006) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/01.mpg.0000221905.68781.4a · Cited by 48 · see citing works
New insight into the pathogenesis of sepsis and the sepsis syndrome
Johnson, G. B., Brunn, G. J., Samstein, B., & Platt, J. L. (2005) · Surgery · doi:10.1016/j.surg.2004.08.001 · Cited by 34 · see citing works
Radulescu, A., Zorko, N. A., Yu, X., & Besner, G. E. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e3181994fa0 · Cited by 32 · see citing works
Harada, K., Toyonaga, A., Mitsuyama, K., Sasaki, E., & Tanikawa, K. (2009) · Digestion · doi:10.1159/000201145 · Cited by 26 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Hemarajata, P., & Versalovic, J. (2013) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756283x12459294 · Cited by 1,083 · see citing works
A Comprehensive Review on the Role of the Gut Microbiome in Human Neurological Disorders
Sorboni, S. G., Moghaddam, H. S., Jafarzadeh-Esfehani, R., & Soleimanpour, S. (2022) · Clinical Microbiology Reviews · doi:10.1128/cmr.00338-20 · Cited by 562 · see citing works
Can probiotics modulate human disease by impacting intestinal barrier function?
Bron, P. A., Kleerebezem, M., Brummer, R.-J., Cani, P. D., Mercenier, A., MacDonald, T. T., Garcia-Ródenas, C. L., & Wells, J. M. (2017) · British Journal Of Nutrition · doi:10.1017/s0007114516004037 · Cited by 499 · see citing works
“lated both intestinal inflammation and barrier outcomes((148,158,165)).”
Autism 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 · see citing works
Oliva, S., Nardo, G. D., Ferrari, F., Mallardo, S., Rossi, P., Patrizi, G., Cucchiara, S., & Stronati, L. (2011) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2011.04939.x · Cited by 280 · see citing works
Hsieh, Y.-Y., Tung, S.-Y., Pan, H.-Y., Yen, C.-W., Xu, H.-W., Lin, Y.-J., Deng, Y.-F., Hsu, W.-T., Wu, C.-S., & Li, C. (2018) · Scientific Reports · doi:10.1038/s41598-017-18596-0 · Cited by 269 · see citing works
Szajewska, H., Gyrczuk, E., & Horvath, A. (2012) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2012.08.004 · Cited by 244 · see citing works
Prebiotics, probiotics, synbiotics, and the immune system: experimental data and clinical evidence
Frei, R., Akdis, M., & O’Mahony, L. (2015) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000151 · Cited by 240 · see citing works
Irritable Bowel Syndrome, Gut Microbiota and Probiotics
Lee, B. J., & Bak, Y. (2011) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm.2011.17.3.252 · Cited by 229 · see citing works
Study and use of the probiotic Lactobacillus reuteri in pigs: a review
Hou, C., Zeng, X., Yang, F., Liu, H., & Qiao, S. (2015) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-015-0014-3 · Cited by 219 · see citing works
Yang, F., Wang, A., Zeng, X., Hou, C., Liu, H., & Qiao, S. (2015) · BMC Microbiology · doi:10.1186/s12866-015-0372-1 · Cited by 216 · see citing works
Porcine IPEC-J2 intestinal epithelial cells in microbiological investigations
Brosnahan, A. J., & Brown, D. R. (2011) · Veterinary Microbiology · doi:10.1016/j.vetmic.2011.10.017 · Cited by 200 · see citing works
Liu, Y., Fatheree, N. Y., Mangalat, N., & Rhoads, J. M. (2011) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00266.2011 · Cited by 181 · see citing works
Self-citationGao, C., Major, A., Rendon, D., Lugo, M., Jackson, V., Shi, Z., Mori-Akiyama, Y., & Versalovic, J. (2015) · mBio · doi:10.1128/mbio.01358-15 · Cited by 176 · see citing works
Infant colic: mechanisms and management
Zeevenhooven, J., Browne, P. D., L’Hoir, M. P., de Weerth, C., & Benninga, M. A. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-018-0008-7 · Cited by 181 · see citing works
Ansari, F., Pourjafar, H., Tabrizi, A., & Homayouni, A. (2020) · Current Pharmaceutical Biotechnology · doi:10.2174/1389201021666200107113812 · Cited by 170 · see citing works
Oh, N. S., Lee, J. Y., Kim, Y.-T., Kim, S. H., & Lee, J.-H. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1785803 · Cited by 166 · see citing works
Intestinal in vitro and ex vivo Models to Study Host-Microbiome Interactions and Acute Stressors
Pearce, S., Coia, H. G., Karl, J. P., Pantoja-Feliciano, I. G., Zachos, N. C., & Racicot, K. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01584 · Cited by 159 · see citing works
Can probiotics benefit children with autism spectrum disorders?
Navarro, F., Liu, Y., & Rhoads, J. M. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i46.10093 · Cited by 154 · see citing works
Self-citationMicrobial lysate upregulates host oxytocin
Varian, B. J., Poutahidis, T., DiBenedictis, B. T., Levkovich, T., Ibrahim, Y., Didyk, E., Shikhman, L., Cheung, H. K., Hardas, A., Ricciardi, C. E., et al. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.11.002 · Cited by 153 · see citing works
Gurunathan, S., Pratheep, T., & Kim, J. (2023) · Foods · doi:10.3390/foods13010089 · Cited by 139 · see citing works
Szkaradkiewicz, A. K., Stopa, J., & Karpiński, T. M. M. (2014) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-014-0277-y · Cited by 140 · see citing works
Role of probiotics and prebiotics in immunomodulation
Yahfoufi, N., Mallet, J., Graham, É. A., & Matar, C. (2018) · Current Opinion in Food Science · doi:10.1016/j.cofs.2018.04.006 · Cited by 135 · see citing works
Cassani, L., Gomez-Zavaglia, A., & Simal-Gandara, J. (2020) · Food Research International · doi:10.1016/j.foodres.2019.108852 · Cited by 133 · see citing works
Lactobacillus reuteri Strain Combination In Helicobacter pylori Infection
Francavilla, R., Polimeno, L., Demichina, A., Maurogiovanni, G., Principi, M., Scaccianoce, G., Ierardi, E., Russo, F., Riezzo, G., Leo, A. D., et al. (2013) · Journal of Clinical Gastroenterology · doi:10.1097/mcg.0000000000000007 · Cited by 125 · see citing works
Urbańska, M., & Szajewska, H. (2014) · European Journal of Pediatrics · doi:10.1007/s00431-014-2328-0 · Cited by 125 · see citing works
Serotonin as a link between the gut-brain-microbiome axis in autism spectrum disorders
Israelyan, N., & Margolis, K. G. (2018) · Pharmacological Research · doi:10.1016/j.phrs.2018.03.020 · Cited by 122 · see citing works
Gao, C., Ganesh, B. P., Shi, Z., Shah, R. R., Fultz, R., Major, A., Venable, S., Lugo, M., Hoch, K., Chen, X., et al. (2017) · The American Journal of Pathology · doi:10.1016/j.ajpath.2017.06.011 · Cited by 122 · see citing works
Lee, J., Yang, W., Hostetler, A., Schultz, N., Suckow, M. A., Stewart, K. L., Kim, D. D., & Kim, H. S. (2016) · BMC Microbiology · doi:10.1186/s12866-016-0686-7 · Cited by 107 · see citing works
Wang, G., Huang, S., Cai, S., Yu, H., Wang, Y., Zeng, X., & Qiao, S. (2020) · Nutrients · doi:10.3390/nu12082298 · Cited by 107 · see citing works
Matsuda, Y., Ozawa, N., Shinozaki, T., Wakabayashi, K.-I., Suzuki, K., Kawano, Y., Ohtsu, I., & Tatebayashi, Y. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0855-1 · Cited by 105 · see citing works
Yang, I., Eibach, D., Kops, F., Brenneke, B., Woltemate, S., Schulze, J., Bleich, A., Gruber, A. D., Muthupalani, S., Fox, J. G., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070783 · Cited by 104 · see citing works
Javanshir, N., Hosseini, G. N. G., Sadeghi, M., Esmaeili, R., Satarikia, F., Ahmadian, G., & Fard, N. A. (2021) · Biological Procedures Online · doi:10.1186/s12575-021-00160-w · Cited by 109 · see citing works
Jiang, X., Gu, S., Liu, D., Zhao, L., Xia, S., He, X., Chen, H., & Ge, J. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02425 · Cited by 103 · see citing works
Probiotics for infantile colic: a systematic review
Anabrees, J., Indrio, F., Paes, B. A., & AlFaleh, K. M. (2013) · BMC Pediatrics · doi:10.1186/1471-2431-13-186 · Cited by 102 · see citing works
Urbańska, M., Gieruszczak‐Białek, D., & Szajewska, H. (2016) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.13590 · Cited by 101 · see citing works
Characterization of Intestinal Lactobacillus reuteri Strains as Potential Probiotics
Singh, T. P., Kaur, G., Malik, R. K., Schillinger, U., Guigas, C., & Kapila, S. (2012) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-012-9090-2 · Cited by 98 · see citing works
Roselli, M., Pieper, R., Rogel-Gaillard, C., de Vries, H., Bailey, M., Smidt, H., & Lauridsen, C. (2017) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2017.07.011 · Cited by 98 · see citing works
Benefits of probiotics on enteral nutrition in preterm neonates: a systematic review
Athalye‐Jape, G., Deshpande, G. C., Rao, S. C., & Patole, S. (2014) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.092551 · Cited by 95 · see citing works
Plaza‐Díaz, J., Ruiz‐Ojeda, F. J., Gil‐Campos, M., & Gil, Á. (2018) · Nutrients · doi:10.3390/nu10010042 · Cited by 90 · see citing works
Liu, Y., Fatheree, N. Y., Dingle, B. M., Tran, D. Q., & Rhoads, J. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056547 · Cited by 87 · see citing works
Self-citationReprint of: Serotonin as a link between the gut-brain-microbiome axis in autism spectrum disorders
Israelyan, N., & Margolis, K. G. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2018.12.023 · Cited by 87 · see citing works
Liu, Y.-Y., Tian, X.-J., He, B., Hoang, T. K., Taylor, C. M., Blanchard, E. E., Freeborn, J., Park, S., Luo, M., Couturier, J. P., et al. (2019) · American Journal of Physiology - Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00107.2019 · Cited by 90 · see citing works
Self-citationThe Promising Role of Probiotics in Managing the Altered Gut in Autism Spectrum Disorders
Abdellatif, B., McVeigh, C., Bendriss, G., & Châari, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21114159 · Cited by 84 · see citing works
Wu, R., Pasyk, M., Wang, B., Forsythe, P., Bienenstock, J., Mao, Y., Sharma, P., Stanisz, A. M., & Kunze, W. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12072 · Cited by 84 · see citing works
Liu, Y., Tran, D. Q., Fatheree, N. Y., & Rhoads, J. M. (2014) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00038.2014 · Cited by 78 · see citing works
Self-citationInfantile Colic Is Associated With Low‐grade Systemic Inflammation
Pärtty, A., Kalliomäki, M. A., Salminen, S., & Isolauri, E. (2016) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001340 · Cited by 78 · see citing works
Fusobacterium nucleatum predicts a high risk of metastasis for esophageal squamous cell carcinoma
Shi, C., Li, Z., Zheng, J., 孔为民, Fan, T., Jian, D., Cheng, X., Zhao, H., Ma, J., Tang, H., et al. (2021) · BMC Microbiology · doi:10.1186/s12866-021-02352-6 · Cited by 73 · see citing works
Haileselassie, Y., Navis, M., Vu, N., Qazi, K. R., Réthi, B., & Sverremark‐Ekström, E. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00096 · Cited by 72 · see citing works
Wang, Y., Ma, R., Liu, F., Lee, S. A., & Zhang, L. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00374 · Cited by 71 · see citing works
Lactobacillus reuteri ATCC55730 in Cystic Fibrosis
Nardo, G. D., Oliva, S., Menichella, A., Pistelli, R., Biase, R. V. D., Patriarchi, F., Cucchiara, S., & Stronati, L. (2013) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000000187 · Cited by 71 · see citing works
Hod, K., Sperber, A. D., Ron, Y., Boaz, M., Dickman, R. M., Berliner, S. A., Halpern, Z., Maharshak, N., & Dekel, R. (2017) · Neurogastroenterology & Motility · doi:10.1111/nmo.13037 · Cited by 70 · see citing works
Fatheree, N. Y., Liu, Y., Taylor, C. M., Hoang, T. K., Cai, C. C., Rahbar, M. H., Hessabi, M., Ferris, M. J., McMurtry, V., Wong, C., et al. (2017) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2017.07.036 · Cited by 73 · see citing works
Self-citationProbiotics and gut health: linking gut homeostasis and poultry productivity
Shini, S., & Bryden, W. L. (2021) · Animal Production Science · doi:10.1071/an20701 · Cited by 68 · see citing works
Erdman, S. E., & Poutahidis, T. (2016) · International review of neurobiology · doi:10.1016/bs.irn.2016.07.004 · Cited by 67 · see citing works
Fijan, S., Šulc, D., & Steyer, A. (2018) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph15071539 · Cited by 67 · see citing works
Lactobacillus reuteri DSM 17938 as a Probiotic for Preterm Neonates
Athalye‐Jape, G., Rao, S. C., & Patole, S. (2015) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607115588113 · Cited by 66 · see citing works
Ganesh, B. P., Hall, A., Ayyaswamy, S., Nelson, J. W., Fultz, R., Major, A. M., Haag, A. M., Esparza, M., Lugo, M., Venable, S. F., et al. (2017) · Mucosal Immunology · doi:10.1038/mi.2017.58 · Cited by 65 · see citing works
Probiotic Supplementation in Preterm: Feeding Intolerance and Hospital Cost
Indrio, F., Riezzo, G., Tafuri, S., Ficarella, M., Carlucci, B., Bisceglia, M., Polimeno, L., & Francavilla, R. (2017) · Nutrients · doi:10.3390/nu9090965 · Cited by 65 · see citing works
Yi, H., Wang, L., Xiong, Y., Wang, Z., Qiu, Y., Wen, X., Jiang, Z., Yang, X., & Ma, X. (2018) · Mediators of Inflammation · doi:10.1155/2018/6434910 · Cited by 64 · see citing works
Karimi, S., Jonsson, H., Lundh, T., & Roos, S. (2018) · Physiological Reports · doi:10.14814/phy2.13514 · Cited by 62 · see citing works
Olson, J. K., Navarro, J. B., Allen, J. M., McCulloh, C. J., Mashburn‐Warren, L., Wang, Y., Varaljay, V. A., Bailey, M. T., Goodman, S. D., & Besner, G. E. (2018) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00078.2018 · Cited by 61 · see citing works
Intestinal Dysbiosis and the Developing Lung: The Role of Toll-Like Receptor 4 in the Gut-Lung Axis
Wedgwood, S., Gerard, K., Halloran, K., Hanhauser, A., Monacelli, S., Warford, C., Thai, P. N., Chiamvimonvat, N., Lakshminrusimha, S., Steinhorn, R. H., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00357 · Cited by 59 · see citing works
Mangalat, N., Liu, Y., Fatheree, N. Y., Ferris, M. J., Arsdall, M. R. V., Chen, Z., Rahbar, M. H., Gleason, W. A., Norori, J., Tran, D. Q., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043910 · Cited by 58 · see citing works
Self-citationCui, S., Hu, M., Sun, Y., Mao, B., Zhang, Q., Zhao, J., Tang, X., & Zhang, H. (2022) · Microorganisms · doi:10.3390/microorganisms11010048 · Cited by 58 · see citing works
Weirdt, R. D., Crabbé, A., Roos, S., Vollenweider, S., Lacroix, C., van Pijkeren, J. P., Britton, R. A., Sarker, S. F., de Wiele, T. V., & Nickerson, C. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037116 · Cited by 58 · see citing works
Probiotics for oral health: a critical evaluation of bacterial strains
Beattie, R. E. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1430810 · Cited by 56 · see citing works
Lactobacillus reuteri CRL 1101 highly produces mannitol from sugarcane molasses as carbon source
Ortiz, M. E., Fornaguera, M. J., Raya, R. R., & Mozzi, F. (2012) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-012-3945-z · Cited by 56 · see citing works
Cousin, F., Foligné, B., Deutsch, S., Massart, S., Parayre, S., Loir, Y. L., Boudry, G., & Jan, G. (2012) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf302245m · Cited by 55 · see citing works
Bene, K., Kavanaugh, D. W., Leclaire, C., Gunning, A. P., MacKenzie, D. A., Wittmann, A., Young, I. D., Kawasaki, N., Rajnavölgyi, É., & Juge, N. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00321 · Cited by 55 · see citing works
CO and CO ‐releasing molecules ( CO ‐ RMs ) in acute gastrointestinal inflammation
Babu, D., Motterlini, R., & Lefebvre, R. A. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12632 · Cited by 52 · see citing works
Chapman, J. C., Liu, Y., Zhu, L., & Rhoads, J. M. (2012) · Pediatric Research · doi:10.1038/pr.2012.137 · Cited by 52 · see citing works
Self-citationMurakami, K., Habukawa, C., Nobuta, Y., Moriguchi, N., & Takemura, T. (2012) · BioPsychoSocial Medicine · doi:10.1186/1751-0759-6-16 · Cited by 52 · see citing works
Beversdorf, D. Q., Stevens, H. E., Margolis, K. G., & de Water, J. V. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666191119093335 · Cited by 53 · see citing works
Odamaki, T., Horigome, A., Sugahara, H., Hashikura, N., Minami, J., Xiao, J.-Z., & Abe, F. (2015) · International Journal of Genomics · doi:10.1155/2015/567809 · Cited by 50 · see citing works
Aktaş, B., Wolfe, T. J. D., Safdar, N., Darien, B. J., & Steele, J. L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0156374 · Cited by 48 · see citing works
Pre-protective effect of lipoic acid on injury induced by H2O2 in IPEC-J2 cells
Cai, X., Chen, X., Wang, X., Xu, C., Guo, Q., Zhu, L., Zhu, S., & Xu, J. (2013) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-013-1595-9 · Cited by 44 · see citing works
Smolińska, S., Groeger, D., & O’Mahony, L. (2017) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2016.09.004 · Cited by 44 · see citing works
Chytilová, M., Mudroňová, D., Nemcová, R., Gancarčíková, S., Buleca, V., Koščová, J., & Tkáčiková, Ľ. (2013) · Research in Veterinary Science · doi:10.1016/j.rvsc.2013.02.002 · Cited by 42 · see citing works
Szymański, H., & Szajewska, H. (2019) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0000000000002355 · Cited by 44 · see citing works
Gomes, M. J. C., Martino, H. S. D., & Tako, E. (2021) · Nutrients · doi:10.3390/nu13010189 · Cited by 41 · see citing works
Whary, M. T., Taylor, N. S., Feng, Y., Ge, Z., Muthupalani, S., Versalovic, J. A., & Fox, J. G. (2011) · Immunology · doi:10.1111/j.1365-2567.2011.03423.x · Cited by 41 · see citing works
Degradation potential of bisphenol A by Lactobacillus reuteri
Ju, J., Shen, L., Xie, Y., Yu, H., Guo, Y., Cheng, Y., Qian, H., & Yao, W. (2019) · LWT · doi:10.1016/j.lwt.2019.02.022 · Cited by 40 · see citing works
Lactic acid bacteria in Asian fermented foods and their beneficial roles in human health
Doo, H., Kwak, J., Keum, G. B., Ryu, S., Choi, Y., Kang, J., Kim, H., Chae, Y., Kim, S., Kim, H. B., et al. (2024) · Food Science and Biotechnology · doi:10.1007/s10068-024-01634-9 · Cited by 43 · see citing works
Ammoscato, F., Scirocco, A., Altomare, A., Matarrese, P., Petitta, C., Ascione, B., Caronna, R., Guarino, M. P. L., Marignani, M., Cicala, M., et al. (2013) · Neurogastroenterology & Motility · doi:10.1111/nmo.12232 · Cited by 37 · see citing works
Krill oil, vitamin D and Lactobacillus reuteri cooperate to reduce gut inflammation
Costanzo, M., Cesi, V., Palone, F., Pierdomenico, M., Colantoni, E., Leter, B., Vitali, R., Negroni, A., Cucchiara, S., & Stronati, L. (2018) · Beneficial Microbes · doi:10.3920/bm2017.0078 · Cited by 37 · see citing works
Rahman, Z., Bhale, N. A., Dikundwar, A. G., & Dandekar, M. P. (2023) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-023-10109-y · Cited by 37 · see citing works
Limosilactobacillus reuteri Regulating Intestinal Function: A Review
Jiang, J., Li, K., Xiao, Y., Zhong, A., Tang, J., Duan, Y., & Li, Z. (2022) · Fermentation · doi:10.3390/fermentation9010019 · Cited by 36 · see citing works
Microbiome as an Immunological Modifier
Kumar, M., Singh, P., Murugesan, S., Vétizou, M., McCulloch, J. A., Badger, J. H., Trinchieri, G., & Khodor, S. A. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9773-2_27 · Cited by 36 · see citing works
Farkas, O., Mátis, G., Pászti-Gere, E., Palócz, O., Kulcsár, A., Petrilla, J., Csikó, G., Neogrády, Z., & Gálfi, P. (2014) · Journal of Animal Science · doi:10.2527/jas.2013-7453 · Cited by 34 · see citing works
Chen, L., Zhang, S., Wu, S., Ren, Z., Liu, G., & Wu, J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.696148 · Cited by 33 · see citing works
Current Perspectives on Gastrointestinal Models to Assess Probiotic-Pathogen Interactions
Anjum, M., Laitila, A., Ouwehand, A. C., & Forssten, S. D. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.831455 · Cited by 31 · see citing works
Anders, J. L., Mychajliw, A. M., Moustafa, M. A. M., Mohamed, W. M. A., Hayakawa, T., Nakao, R., & Koizumi, I. (2022) · Ecology and Evolution · doi:10.1002/ece3.9216 · Cited by 29 · see citing works
Probiotics in neonatal intensive care – Back to the future
Deshpande, G. C., Rao, S. C., & Patole, S. (2015) · Australian and New Zealand Journal of Obstetrics and Gynaecology · doi:10.1111/ajo.12328 · Cited by 29 · see citing works
Lee, H. L., Kim, J. M., Moon, J. H., Kim, M. J., Jeong, H. R., Go, M. J., Kim, H., Eo, H. J., Lee, U., & Heo, H. J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms24010090 · Cited by 29 · see citing works
Břicháček, B., Lagenaur, L. A., Lee, P. P., Venzon, D. J., & Hamer, D. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078817 · Cited by 28 · see citing works
The Game for Three: Salmonella–Host–Microbiota Interaction Models
Grzymajło, K. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.854112 · Cited by 26 · see citing works
Probiotics for the Management of Infantile Colic
Szajewska, H., & Dryl, R. (2016) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1002/j.1536-4801.2016.tb00032.x · Cited by 25 · see citing works
Șurlin, P., Nicolae, F. M., Şurlin, V., Pătrașcu, Ș., Ungureanu, B. S., Didilescu, A. C., & Gheonea, D. I. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9123885 · Cited by 25 · see citing works
Phylogenetically diverse bacterial species produce histamine
Engevik, K. A., Hazzard, A. A., Puckett, B., Hoch, K. M., Haidacher, S. J., Haag, A. M., Spinler, J. K., Versalovic, J. A., Engevik, M. A., & Horvath, T. D. (2024) · Systematic and Applied Microbiology · doi:10.1016/j.syapm.2024.126539 · Cited by 23 · see citing works
- Authors
- Liu, Y., Fatheree, N. Y., Mangalat, N., & Rhoads, J. M.
- Affiliations
- The University of Texas Health Science Center at Houston (US)
- Corresponding author
- Rhoads, Jon Marc
- Venue
- American Journal of Physiology-Gastrointestinal and Liver Physiology
- Publisher
- American Physiological Society
- Published
- 2010-11
- Volume
- 299
- Issue
- 5
- Pages
- G1087-G1096
- ISSN
- 0193-1857 (ISSN-L)
- 1522-1547
- PMC
- PMC2993169
- OpenAlex
- W2153949996
- Cited by
- 207
- References
- 36
- Citations by year
- 2026: 13 · 2025: 8 · 2024: 13 · 2023: 9 · 2022: 23 · 2021: 12 · 2020: 12 · 2019: 13 · 2018: 21 · 2017: 12 · 2016: 13 · 2015: 14 · 2014: 6 · 2013: 16 · 2012: 14
- FWCI
- 18.65
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- American Journal of Physiology-Gastrointestinal and Liver Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (DK56338, P30DK056338)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Keywords
- Lactobacillus reuteri, probiotics, intestinal inflammation, lipopolysaccharide, strain-specific effects, interleukin-8, interferon-gamma, IL-13, intestinal epithelial cells, IPEC-J2 cells, IEC-6 cells, cow milk formula, anti-inflammatory activity, pro-inflammatory effects, cytokines
- MeSH terms
- Analysis of Variance, Animals, Animals, Newborn, Cells, Cultured, Epithelial Cells, Humans, Ileum, Inflammation, Intestinal Mucosa, Jejunum, Swine, Interleukin-8, Rats, Sprague-Dawley, Probiotics, Reverse Transcriptase Polymerase Chain Reaction, Rats, Limosilactobacillus reuteri
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