Characterization of the anti-inflammatory Lactobacillus reuteri BM36301 and its probiotic benefits on aged mice
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BACKGROUND: The gut microbiota is playing more important roles in host immune regulation than was initially expected. Since many benefits of microbes are highly strain-specific and their mechanistic details remain largely elusive, further identification of new probiotic bacteria with immunoregulatory potentials is of great interest. RESULTS: We have screened our collection of probiotic lactic acid bacteria (LAB) for their efficacy in modulating host immune response. Some LAB are characterized by suppression of TNF-α induction when LAB culture supernatants are added to THP-1 cells, demonstrating the LAB's anti-inflammatory potential. These suppressive materials were not inactivated by heat or trypsin. On the other hand, treatment of THP-1 directly with live bacterial cells identified a group of pro-inflammatory LAB, which stimulated significant production of TNF-α. Among those, we chose the Lactobacillus reuteri BM36301 as an anti-inflammatory strain and the L. reuteri BM36304 as a pro-inflammatory strain, and further studied their in vivo effects. We supplied C57BL/6 mice with these bacteria in drinking water while feeding them a standard diet for 20 weeks. Interestingly, these L. reuteri strains evoked different consequences depending on the gender of the mice. That is, males treated with anti-inflammatory BM36301 experienced less weight gain and higher testosterone level; females treated with BM36301 maintained lower serum TNF-α as well as healthy skin with active folliculogenesis and hair growth. Furthermore, while males treated with pro-inflammatory BM36304 developed higher serum levels of TNF-α and insulin, in contrast females did not experience such effects from this bacteria strain. CONCLUSION: The L. reuteri BM36301 was selected as an anti-inflammatory strain in vitro. It helped mice maintain healthy conditions as they aged. These findings propose the L. reuteri BM36301 as a potential probiotic strain to improve various aspects of aging issues.
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In aging mice, L. reuteri supplementation resulted in larger testicles and increased serum testosterone compared to age-matched controls.
“Further, aging mice supplemented with the probiotic bacterium L. reuteri had larger testicles and increased serum testosterone levels compared to their age-matched controls [237, 254].”
From International Society of Sports Nutrition Position Stand: Probiotics (2019) · cites this paper as [254]
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Changes of Intestinal Functions in Liver Cirrhosis
Fukui, H., & Wiest, R. (2016) · Inflammatory Intestinal Diseases · doi:10.1159/000444436 · Cited by 6,820 · see citing works
Gut microbiota in health and disease
Sekirov, I., Russell, S. L., Antunes, L. C. M., & Finlay, B. B. (2010) · Physiological Reviews · doi:10.1152/physrev.00045.2009 · Cited by 4,182 · see citing works
Bravo, J. A., Forsythe, P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., Bienenstock, J., & Cryan, J. F. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102999108 · Cited by 3,888 · see citing works
Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43
Maslowski, K. M., Vieira, A. T., Ng, A., Kranich, J., Sierro, F., Yu, D., Schilter, H. C., Rolph, M. S., Mackay, F., Artis, D., et al. (2009) · Nature · doi:10.1038/nature08530 · Cited by 3,241 · see citing works
Role of the gut microbiota in immunity and inflammatory disease
Kamada, N., Seo, S.-U., Chen, G. Y., & Núñez, G. (2013) · Nature reviews. Immunology · doi:10.1038/nri3430 · Cited by 2,256 · see citing works
Chun, J., Lee, J., Jung, Y., Kim, M., Kim, S., Kim, B. K., & Lim, Y. (2007) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijs.0.64915-0 · Cited by 2,096 · see citing works
Self-citationTNF-mediated inflammatory disease
Bradley, Jr. (2008) · The Journal of Pathology · doi:10.1002/path.2287 · Cited by 2,094 · see citing works
THP-1 cell line: An in vitro cell model for immune modulation approach
Chanput, W. P., Mes, J. J., & Wichers, H. J. (2014) · International Immunopharmacology · doi:10.1016/j.intimp.2014.08.002 · Cited by 1,408 · see citing works
Müller-Röver, S., Foitzik, K., Paus, R., Handjiski, B., van der Veen, C., Eichmüller, S., McKay, I. A., & Stenn, K. S. (2001) · Journal of Investigative Dermatology · doi:10.1046/j.0022-202x.2001.01377.x · Cited by 1,375 · see citing works
Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut
Artis, D. (2008) · Nature reviews. Immunology · doi:10.1038/nri2316 · Cited by 1,136 · cited 2× · see citing works
“Local interactions between the gut microbiota and its host primarily involve the direct recognition of bacterial surface molecules by neighboring epithelial cells and immune cells in the intestine [13, 18].”
BackgroundTh17 and regulatory T cells in mediating and restraining inflammation
Littman, D. R., & Rudensky, A. Y. (2010) · Cell · doi:10.1016/j.cell.2010.02.021 · Cited by 1,039 · see citing works
Gut microbes and the brain: paradigm shift in neuroscience
Mayer, E. A., Knight, R., Mazmanian, S. K., Cryan, J. F., & Tillisch, K. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3299-14.2014 · Cited by 1,033 · see citing works
Potential Uses of Probiotics in Clinical Practice
Reid, G., Jaß, J., Sebulsky, M. T., & McCormick, J. K. (2003) · Clinical Microbiology Reviews · doi:10.1128/cmr.16.4.658-672.2003 · Cited by 918 · see citing works
Jacobsen, C. N., Nielsen, V. R., Hayford, A. E., Møller, P. L., Michaelsen, K. F., Pærregaard, A., Sandström, B., Tvede, M., & Jakobsen, M. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.11.4949-4956.1999 · Cited by 880 · see citing works
Yan, F., Cao, H., Cover, T. L., Whitehead, R. H., Washington, M. K., & Polk, D. B. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.11.022 · Cited by 828 · see citing works
Thomas, C. M., Hong, T., van Pijkeren, J. P., Hemarajata, P., Trinh, D. V., Hu, W., Britton, R. A., Kalkum, M., & Versalovic, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031951 · Cited by 491 · see citing works
Immunomodulatory mechanisms of lactobacilli
Wells, J. M. (2011) · Microbial Cell Factories · doi:10.1186/1475-2859-10-s1-s17 · Cited by 431 · see citing works
Bernet‐Camard, M., Brassart, D., Neeser, J., & Servin, A. L. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.12.4121-4128.1993 · Cited by 381 · see citing works
Turroni, F., Ventura, M., Buttó, L. F., Duranti, S., O’Toole, P. W., Motherway, M. O., & van Sinderen, D. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1318-0 · Cited by 336 · see citing works
Shokryazdan, P., Sieo, C. C., Ramasamy, K., Liang, J. B., Alitheen, N. B., Jahromi, M. F., & Ho, Y. W. (2014) · BioMed Research International · doi:10.1155/2014/927268 · Cited by 331 · see citing works
Lactic acid bacteria and their effect on the immune system.
Perdigón, G., Fuller, R., & Raya, R. R. (2001) · PubMed · Cited by 329 · see citing works
The Human Gut Microbiome and Body Metabolism: Implications for Obesity and Diabetes
Devaraj, S., Hemarajata, P., & Versalovic, J. (2013) · Clinical Chemistry · doi:10.1373/clinchem.2012.187617 · Cited by 321 · see citing works
Finding the Missing Links among Metabolites, Microbes, and the Host
Dorrestein, P. C., Mazmanian, S. K., & Knight, R. (2014) · Immunity · doi:10.1016/j.immuni.2014.05.015 · Cited by 317 · see citing works
Ménard, S., Candalh, C., Bambou, J. C., Terpend, K., Cerf–Bensussan, N., & Heyman, M. (2004) · Gut · doi:10.1136/gut.2003.026252 · Cited by 309 · see citing works
Matsumoto, M., Kurihara, S., Kibe, R., Ashida, H., & Benno, Y. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023652 · Cited by 290 · see citing works
McCabe, L. R., Irwin, R., Schaefer, L., & Britton, R. A. (2013) · Journal of Cellular Physiology · doi:10.1002/jcp.24340 · Cited by 274 · see citing works
Antimicrobial Activity – The Most Important Property of Probiotic and Starter Lactic Acid Bacteria
Šušković, J., Kos, B., Beganović, J., Pavunc, A. L., Habjanič, K., & Matošić, S. (2010) · University of Zagreb University Computing Centre (SRCE) · Cited by 271 · see citing works
Nguyen, V. D., Hatahet, F., Salo, K. E., Enlund, E., Zhang, C., & Ruddock, L. W. (2011) · Microbial Cell Factories · doi:10.1186/1475-2859-10-1 · Cited by 260 · see citing works
Anti-Obesity Effect of Lactobacillus gasseri BNR17 in High-Sucrose Diet-Induced Obese Mice
Kang, J.-H., Yun, S.-I., Park, M.-H., Park, J.-H., Jeong, S.-Y., & Park, H.-O. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054617 · Cited by 230 · see citing works
Leydig cell aging and the mechanisms of reduced testosterone synthesis.
Midzak, A. S., Chen, H., Papadopoulos, V., & Zirkin, B. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.07.016 · Cited by 218 · see citing works
Gut Microbial Flora, Prebiotics, and Probiotics in IBD: Their Current Usage and Utility
Scaldaferri, F., Gerardi, V., Lopetuso, L. R., Zompo, F. D., Mangiola, F., Boškoski, I., Bruno, G., Petito, V., Laterza, L., Cammarota, G., et al. (2013) · BioMed Research International · doi:10.1155/2013/435268 · Cited by 207 · see citing works
Human-derived probiotic Lactobacillus reuteri strains differentially reduce intestinal inflammation
Liu, Y., Fatheree, N. Y., Mangalat, N., & Rhoads, J. M. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00124.2010 · Cited by 207 · see citing works
Gender differences in skin: A review of the literature
Dao, H., & Kazin, R. A. (2007) · Gender Medicine · doi:10.1016/s1550-8579(07)80061-1 · Cited by 199 · see citing works
Probiotics from research to market: the possibilities, risks and challenges
Foligné, B., Daniel, C., & Pot, B. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.06.008 · Cited by 197 · see citing works
Probiotic Bacteria Induce a ‘Glow of Health’
Levkovich, T., Poutahidis, T., Smillie, C. S., Varian, B. J., Ibrahim, Y. M., Lakritz, J. R., Alm, E. J., & Erdman, S. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053867 · Cited by 196 · see citing works
Imaoka, A., Shima, T., Kato, K., Mizuno, S., Uehara, T., Matsumoto, S., Setoyama, H., Hara, T., & Umesaki, Y. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.2511 · Cited by 179 · see citing works
Probiotic Microbes Sustain Youthful Serum Testosterone Levels and Testicular Size in Aging Mice
Poutahidis, T., Springer, A., Levkovich, T., Qi, P., Varian, B. J., Lakritz, J. R., Ibrahim, Y. M., Chatzigiagkos, A., Alm, E. J., & Erdman, S. E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0084877 · Cited by 177 · see citing works
Microbial Reprogramming Inhibits Western Diet-Associated Obesity
Poutahidis, T., Kleinewietfeld, M., Smillie, C., Levkovich, T., Perrotta, A., Bhela, S., Varian, B. J., Ibrahim, Y. M., Lakritz, J. R., Kearney, S. M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068596 · Cited by 164 · see citing works
Watanabe, T., Nishio, H., Tanigawa, T., Yamagami, H., Okazaki, H., Watanabe, K., Tominaga, K., Fujiwara, Y., Oshitani, N., Asahara, T., et al. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90553.2008 · Cited by 160 · see citing works
In vitro adhesion assays for probiotics and their in vivo relevance: a review
Ouwehand, A. C., & Salminen, S. (2003) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v15i4.7958 · Cited by 129 · see citing works
The Use of Probiotics in Gastrointestinal Disease
Madsen, K. L. (2001) · Canadian Journal of Gastroenterology · doi:10.1155/2001/690741 · Cited by 125 · see citing works
Adhesion of Lactic Acid Bacteria to Caco‐2 Cells and Their Effect on Cytokine Secretion
Morita, H., He, F., Fuse, T., Ouwehand, A. C., Hashimoto, H., Hosoda, M., Mizumachi, K., & Kurisaki, J. (2002) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2002.tb02698.x · Cited by 121 · see citing works
Toward Effective Probiotics for Autism and Other Neurodevelopmental Disorders
Gilbert, J. A., Krajmalnik‐Brown, R., Porazinska, D. L., Weiss, S. J., & Knight, R. D. (2013) · Cell · doi:10.1016/j.cell.2013.11.035 · Cited by 120 · see citing works
Hörmannsperger, G., & Haller, D. (2009) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2009.08.006 · Cited by 100 · 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
Hemarajata, P., Gao, C., Pflughoeft, K. J., Thomas, C. M., Saulnier, D. M. A., Spinler, J. K., & Versalovic, J. A. (2013) · Journal of Bacteriology · doi:10.1128/jb.00261-13 · Cited by 66 · see citing works
Probiotics: The Scientific Evidence in the Context of Inflammatory Bowel Disease
Celiberto, L. S., Bedani, R., Rossi, E. A., & Cavallini, D. (2015) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2014.941457 · Cited by 64 · see citing works
Probiotic ‘glow of health’: it's more than skin deep
Erdman, S. E., & Poutahidis, T. (2014) · Beneficial Microbes · doi:10.3920/bm2013.0042 · Cited by 56 · see citing works
The Human Microbiome and Probiotics: Implications for Pediatrics
Hsieh, M. H., & Versalovic, J. A. (2008) · Current problems in pediatric and adolescent health care · doi:10.1016/j.cppeds.2008.09.001 · Cited by 48 · see citing works
The Human Microbiome and Probiotics: Implications for Pediatrics
Versalovic, J. A. (2013) · Annals of Nutrition and Metabolism · doi:10.1159/000354899 · Cited by 43 · see citing works
Karunasena, E., McMahon, K. W., Chang, D., & Brashears, M. M. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.01229-14 · Cited by 33 · see citing works
Immunomodulation of Monocytes by Probiotic and Selected Lactic Acid Bacteria
Jensen, H., Drømtorp, S. M., Axelsson, L. T., & Grimmer, S. (2014) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-014-9174-2 · Cited by 32 · see citing works
Flagged first, then by citations
1 of the 53 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Role of Lactobacillus reuteri in Human Health and Diseases
Mu, Q., Tavella, V. J., & Luo, X. M. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00757 · Cited by 744 · see citing works
Roles and applications of probiotic Lactobacillus strains
Zhang, Z., Lv, J., Pan, L., & Zhang, Y. (2018) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-018-9217-9 · Cited by 296 · see citing works
International Society of Sports Nutrition Position Stand: Probiotics
Jäger, R., Mohr, A. E., Carpenter, K. C., Kerksick, C. M., Purpura, M., Moussa, A., Townsend, J. R., Lamprecht, M., West, N. P., Black, K., et al. (2019) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-019-0329-0 · Cited by 277 · see citing works
Pearson-Leary, J., Zhao, C., Bittinger, K., Eacret, D., Luz, S., Vigderman, A. S., Dayanim, G., & Bhatnagar, S. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0380-x · Cited by 206 · see citing works
Effect of Bacillus subtilis Strains on Intestinal Barrier Function and Inflammatory Response
Rhayat, L., Maresca, M., Nicoletti, C., Perrier, J., Brinch, K. S., Christian, S., Devillard, E., & Eckhardt, E. R. M. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00564 · Cited by 178 · see citing works
The "Gut Feeling": Breaking Down the Role of Gut Microbiome in Multiple Sclerosis
Freedman, S. N., Shahi, S. K., & Mangalam, A. K. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0588-x · Cited by 168 · see citing works
Ayyash, M. M., Abdalla, A. K., Alkalbani, N. S., Baig, M. A., Turner, M. S., Liu, S., & Shah, N. P. (2021) · Journal of Dairy Science · doi:10.3168/jds.2021-20398 · Cited by 161 · see citing works
Microbial 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
da Silva, T. F., Glória, R. D. A., Americo, M. F., Freitas, A. D. S., de Jesus, L. C. L., Barroso, F. A. L., Laguna, J. G., Coelho-Rocha, N. D., Tavares, L. M., le Loir, Y., et al. (2024) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-024-10247-x · Cited by 117 · see citing works
Probiotics for the airways: Potential to improve epithelial and immune homeostasis
Martens, K., Pugin, B., Boeck, I. D., Spacova, I., Steelant, B., Seys, S., Lebeer, S., & Hellings, P. W. (2018) · Allergy · doi:10.1111/all.13495 · Cited by 94 · see citing works
Revealing the secret life of skin ‐ with the microbiome you never walk alone
Sfriso, R., Egert, M., Gempeler, M., Voegeli, R., & Campiche, R. (2019) · International Journal of Cosmetic Science · doi:10.1111/ics.12594 · Cited by 90 · see citing works
Melatonin Alleviates Neuroinflammation and Metabolic Disorder in DSS-Induced Depression Rats
Lv, W., Liu, C., Yu, L., Zhou, J., Li, Y., Xiong, Y., Guo, A., Chao, L., Qu, Q., Guang-wei, W., et al. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/1241894 · Cited by 85 · see citing works
Limosilactobacillus reuteri in immunomodulation: molecular mechanisms and potential applications
Luo, Z., Chen, A., Xie, A., Liu, X., Jiang, S., & Yu, R. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1228754 · Cited by 82 · see citing works
Probiotics in Extraintestinal Diseases: Current Trends and New Directions
Kiousi, D. E., Karapetsas, A., Karolidou, K., Panayiotidis, M. I., Pappa, A., & Galanis, Α. (2019) · Nutrients · doi:10.3390/nu11040788 · Cited by 80 · see citing works
Song, X., Wang, W., Ding, S., Liu, X., Wang, Y., & Ma, H. (2021) · Journal of Affective Disorders · doi:10.1016/j.jad.2021.04.037 · Cited by 66 · see citing works
Devi, S. M., Kurrey, N. K., & Halami, P. M. (2018) · Journal of Functional Foods · doi:10.1016/j.jff.2018.05.036 · Cited by 66 · see citing works
Probiotics and their role in gastrointestinal cancers prevention and treatment; an overview.
Javanmard, A., Ashtari, S., Sabet, B., Davoodi, S. H., Rostami‐Nejad, M., Akbari, M. E., Niaz, A., & Mortazavian, A. M. (2018) · Gastroenterology and hepatology from bed to bench. · Cited by 65 · see citing works
Role of Probiotics, Prebiotics, and Synbiotics in the Elderly: Insights Into Their Applications
Ale, E. C., & Binetti, A. G. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.631254 · Cited by 64 · see citing works
Firmicutes in Gut Microbiota Correlate with Blood Testosterone Levels in Elderly Men
Matsushita, M., Fujita, K., Motooka, D., Hatano, K., Hata, J., Nishimoto, M., Banno, E., Takezawa, K., Fukuhara, S., Kiuchi, H., et al. (2022) · The World Journal of Men s Health · doi:10.5534/wjmh.210190 · Cited by 63 · see citing works
Lv, W.-J., Wu, X.-L., Chen, W.-Q., Li, Y.-F., Zhang, G.-F., Chao, L.-M., Zhou, J.-H., Guo, A., Liu, C., & Guo, S.-N. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/7902874 · Cited by 61 · see citing works
Oxidative Stress and Gut Microbiome in Inflammatory Skin Diseases
Ni, Q., Zhang, P., Li, Q., & Han, Z. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.849985 · Cited by 57 · see citing works
Probiotic bacteria as modulators of cellular senescence: emerging concepts and opportunities
Sharma, R., & Padwad, Y. S. (2019) · Gut Microbes · doi:10.1080/19490976.2019.1697148 · Cited by 56 · see citing works
Nekouian, R., Rasouli, B., Ghadimi‐Daresajini, A., & Iragian, G.-R. (2017) · Journal of Cancer Research and Therapeutics · doi:10.4103/0973-1482.204897 · Cited by 53 · see citing works
Yokota, Y., Shikano, A., Kuda, T., Takei, M., Takahashi, H., & Kimura, B. (2018) · International Immunopharmacology · doi:10.1016/j.intimp.2018.01.020 · Cited by 52 · see citing works
Resilience or susceptibility to traumatic stress: Potential influence of the microbiome
Tanelian, A., Nankova, B. B., Miari, M., Nahvi, R. J., & Sabban, E. L. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100461 · Cited by 51 · see citing works
Huang, L., Lv, X., Ze, X., Ma, Z., Zhang, X., He, R., Fan, J., Zhang, M., Sun, B., Wang, F., et al. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.990465 · Cited by 46 · see citing works
Danilenko, V., Devyatkin, A., Marsova, M., Shibilova, M., Ilyasov, R. A., & Shmyrev, V. (2021) · Journal of Inflammation Research · doi:10.2147/jir.s333887 · Cited by 53 · see citing works
Kang, Y.-M., Hong, C.-H., Kang, S.-H., Seo, D.-S., Kim, S.-O., Lee, H.-Y., Sim, H.-J., & An, H.-J. (2020) · Journal of Functional Biomaterials · doi:10.3390/jfb11010003 · Cited by 45 · see citing works
la Fuente, M. D. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-201587 · Cited by 43 · see citing works
Probiotics against airway allergy: host factors to consider
Spacova, I., Ceuppens, J. L., Seys, S., Petrova, M., & Lebeer, S. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.034314 · Cited by 38 · see citing works
Jang, A.-Y., Rod–in, W., Monmai, C., Sohn, M., Kim, T., Jeon, M.-G., & Park, W. J. (2021) · Journal of Applied Microbiology · doi:10.1111/jam.15331 · Cited by 38 · see citing works
Mârza, S. M., Munteanu, C., Papuc, I., Radu, L., & Purdoiu, R. C. (2025) · Animals · doi:10.3390/ani15202986 · Cited by 45 · see citing works
Al-Balawi, M., & Morsy, F. M. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.02017 · Cited by 34 · see citing works
Contribution of gut microbiota to drug-induced liver injury
Chu, H., Ai, Y., Cheng, Z., Yang, L., & Hou, X. (2023) · Hepatobiliary & pancreatic diseases international · doi:10.1016/j.hbpd.2023.06.008 · Cited by 35 · see citing works
Cao, L., Wu, X., Bai, Y. L., Wu, X., & Gu, S. (2019) · Livestock Science · doi:10.1016/j.livsci.2019.03.009 · Cited by 32 · see citing works
Liu, M., Liu, W., Zhang, W., Yao, J., & Mo, X. (2021) · Food Science & Nutrition · doi:10.1002/fsn3.2318 · Cited by 32 · see citing works
Emerging Relationship between the Gut Microbiome and Prostate Cancer
Matsushita, M., Fujita, K., Hatano, K., Velasco, M. A. D., Tsujimura, A., Uemura, H., & Nonomura, N. (2023) · The World Journal of Men s Health · doi:10.5534/wjmh.220202 · Cited by 31 · see citing works
Zhang, Y.-D., Shi, D., Liao, B.-B., Li, Y., Zhang, S., Gao, J., Lin, L., & Wang, Z. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02424-9 · Cited by 30 · see citing works
Freire, M. O. D. L., do Nascimento, L. C. P., de Oliveira, K. Á. R., de Oliveira, A. M., Lima, M. D. S., Napoleão, T. H., Silva, J. H. D. C., Lagranha, C. J., de Souza, E. L., & Alves, J. L. D. B. (2021) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-021-09878-1 · Cited by 30 · see citing works
Sharma, R., Diwan, B., Sharma, A., & Witkowski, J. M. (2022) · Biogerontology · doi:10.1007/s10522-022-09995-6 · Cited by 29 · see citing works
Rohith, H. S., & Halami, P. M. (2021) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-021-09851-y · Cited by 27 · see citing works
Kim, H., Shin, J., Kim, S., Kim, S., Cho, B., Park, S., Park, G., Shin, H., Park, M. S., & Kim, J. (2022) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2022.03.024 · Cited by 26 · see citing works
Self-citationNew lactic acid bacteria for skin health via oral intake of heat-killed or live cells
Kimoto‐Nira, H. (2018) · Animal Science Journal · doi:10.1111/asj.13017 · Cited by 25 · see citing works
Zhan, S., Wu, L., Lv, Y., Huang, W., Ge, C., Hu, Z., Shen, X., Lin, G., Yu, D., & Liu, B. (2025) · Poultry Science · doi:10.1016/j.psj.2025.104997 · Cited by 25 · see citing works
Shibayama, J., Kuda, T., Shikano, A., Fukunaga, M., Takahashi, H., Kimura, B., & Ishizaki, S. (2018) · Food Bioscience · doi:10.1016/j.fbio.2018.07.002 · Cited by 25 · see citing works
Gut microbiome engineering with probiotics: current trends and future directions
Duhan, P., Gupta, B., Ahmed, M. M. M., & Bansal, P. (2025) · Discover Applied Sciences · doi:10.1007/s42452-025-07622-w · Cited by 24 · see citing works
Jiang, P., Yang, W., Jin, Y.-B., Huang, H., Shi, C., Jiang, Y., Wang, J., Kang, Y., Wang, C., & Yang, G. (2019) · Microbial Pathogenesis · doi:10.1016/j.micpath.2019.103754 · Cited by 24 · see citing works
Self-citationWang, Z., Du, J., Ma, W., Diao, X., Liu, Q., & Liu, G. (2024) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-024-13228-w · Cited by 23 · see citing works
Liu, J., Zhu, R., Song, J., Sohaib, M., Wang, S., Mao, J., Qi, J., Xiong, X., Zhou, W., & Guo, L. (2023) · Nutrition Research · doi:10.1016/j.nutres.2023.06.004 · Cited by 23 · see citing works
Shi, R., Jin, Y., Fan, H., Hu, X., Wu, X., Wang, D., Zhao, B., Dai, X., & Liu, X. (2024) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.3c07041 · Cited by 19 · see citing works
Lambert, L., Nováková, M., Lukac, P., Cechova, D., Súkeníková, L., Hrdý, J., Mlček, M., Chlup, H., Suchý, T., & Grus, T. (2019) · BioMed Research International · doi:10.1155/2019/5301405 · Cited by 19 · see citing works
Liu, T., Zhou, L., Li, X., Wei, S., Liu, Y., Wu, S., Wang, P., Dai, X., & Shi, L. S. (2024) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.4c00372 · Cited by 19 · see citing works
Tanelian, A., Nankova, B. B., Miari, M., & Sabban, E. L. (2024) · Biology of Sex Differences · doi:10.1186/s13293-024-00590-7 · Cited by 17 · see citing works
Hu, W., Rajendran, P., Tzang, B., Yeh, Y., Shen, C.-Y., Chen, R., Ho, T., Padma, V. V., Chen, Y.-H., & Huang, C. (2017) · PLoS ONE · doi:10.1371/journal.pone.0185098 · Cited by 17 · see citing works
Parodi, G., Leite, G., Pimentel, M. L., Barlow, G. M., Fiorentino, A., Morales, W., Pimentel, M., Weitsman, S. R., & Mathur, R. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.897283 · Cited by 16 · see citing works
Wu, Z., & Wang, H. X. (2018) · SN Comprehensive Clinical Medicine · doi:10.1007/s42399-018-0033-4 · Cited by 16 · see citing works
Efficacy of probiotics in hair growth and dandruff control: A systematic review and meta-analysis
Yin, C.-S., Nguyen, T. T. M., Yi, E.-J., Zheng, S., Bellere, A. D., Zheng, Q., Jin, X., Kim, M., Park, S., Oh, S., et al. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e29539 · Cited by 15 · see citing works
Han, W., Zheng, Y., Wang, L., & An, C. (2023) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2023.578172 · Cited by 15 · see citing works
Gao, X., Yu, J., Chang, L., Wang, Y., Sun, X., Mu, G., & Qian, F. (2023) · Food Bioscience · doi:10.1016/j.fbio.2023.102512 · Cited by 15 · see citing works
Jendraszak, M., Skibińska, I., Kotwicka, M., & Andrusiewicz, M. (2024) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/10408363.2024.2331489 · Cited by 14 · see citing works
Mechanistic Role of Probiotics in Improving Skin Health
Sharma, G., Khanna, G., Sharma, P., Deol, P. K., & Kaur, I. P. (2021) · Springer eBooks · doi:10.1007/978-981-16-5628-6_2 · Cited by 12 · see citing works
Zhang, C., Yao, D., Su, Z.-N., Chen, H., Hao, P., Liao, Y., Guo, Y., & De-ji, Y. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.739348 · Cited by 12 · see citing works
Identification of Indicative Gut Microbial Guilds in a Natural Aging Mouse Model
Koh, Y., Kuo, L., Tung, Y., Weerawatanakorn, M., & Pan, M. (2023) · ACS Omega · doi:10.1021/acsomega.3c05949 · Cited by 11 · see citing works
Feng, Y., Wu, Y., Wang, J., Dong, Z., Yu, Q., Xia, S., Liu, C., Wang, H., & Wu, X. (2024) · Science China Life Sciences · doi:10.1007/s11427-023-2562-9 · Cited by 11 · see citing works
Wang, Z., Shi, L. S., Li, H., Wei, S., Li, J., & Yuan, L. (2022) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.2c04526 · Cited by 11 · see citing works
Li, W., He, H., Li, S., Jiang, B., Liu, C., Huang, Y., & Su, Y. (2024) · Aquaculture Reports · doi:10.1016/j.aqrep.2024.101976 · Cited by 10 · see citing works
Ye, G.-C., Peng, H., Xiang, J.-C., Miao, L.-T., Liu, C., Wang, S., & Xia, Q. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-024-05937-7 · Cited by 10 · see citing works
Induction of gut Lactobacillus reuteri in normal ICR mice by oral administration of L. plantarum AN1
Yokota, Y., Haraguchi, Y., Shikano, A., Kuda, T., Takahashi, H., & Kimura, B. (2018) · Journal of Food Biochemistry · doi:10.1111/jfbc.12589 · Cited by 10 · see citing works
Kavanová, K., Kostovová, I., Morávková, M., Kubasová, T., Babák, V., & Crhánová, M. (2024) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-024-10259-7 · Cited by 9 · see citing works
Exploring the microbiome-gut-testis axis in testicular germ cell tumors
Čierniková, S., Ševčíková, A., & Mego, M. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1529871 · Cited by 9 · see citing works
A Review of foods and food supplements increasing testosterone levels
Kataoka, T., Hotta, Y., & Kimura, K. (2021) · Journal of Men s Health · doi:10.31083/jomh.2021.008 · Cited by 9 · see citing works
Liu, M., Liu, W., Zhang, W., Niu, J., & Yao, J. (2022) · BioMed Research International · doi:10.1155/2022/2228632 · Cited by 9 · see citing works
Zimmerman, T., Gyawali, R., & Ibrahim, S. A. (2017) · Biotechnology Letters · doi:10.1007/s10529-017-2380-8 · Cited by 9 · see citing works
Xu, S., Cheng, J., Meng, X., Xu, Y., & Mu, Y. (2020) · Evolutionary Bioinformatics · doi:10.1177/1176934320942192 · Cited by 9 · see citing works
A Prerequisite for Health: Probiotics
Rossoni, R. D., Ribeiro, F. D. C., de Barros, P. P., Mylonakis, E. E., & Junqueira, J. C. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-816664-2.00011-6 · Cited by 9 · see citing works
Oral Administration of Lactilactobacillus curvatus LB-P9 Promotes Hair Regeneration in Mice
Song, M., Shim, J., & Song, K. (2023) · Food Science of Animal Resources · doi:10.5851/kosfa.2023.e74 · Cited by 7 · see citing works
The Ageing Gut–Brain study: Exploring the role of the gut microbiota in dementia
Johnstone, A. M., Donaldson, A. I. C., Scott, K. P., & Myint, P. K. (2019) · Nutrition Bulletin · doi:10.1111/nbu.12378 · Cited by 7 · see citing works
A PRISMA Systematic Review of Sexual Dysfunction and Probiotics with Pathophysiological Mechanisms
Yang, S.-J., Nguyen, T. T. M., Jin, X., Zheng, Q., Park, S.-J., Yi, G.-S., & Yi, T. (2025) · Biology · doi:10.3390/biology14030286 · Cited by 6 · see citing works
Probiotics for Management of Gastrointestinal Cancers
Rai, N., Singh, S. P., Keshri, P. K., Barik, S., Kamble, S. C., Singh, S. K., Kumar, R., Mishra, P., Kotiya, D., & Gautam, V. (2020) · Springer eBooks · doi:10.1007/978-981-15-8214-1_9 · Cited by 6 · see citing works
Zaki, R. M., Ramasamy, K., Alwi, N. A. A., Yusoff, R. M., & Lim, S. M. (2022) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-022-10009-7 · Cited by 6 · see citing works
Johari, B., Maghsood, F., Madanchi, H., Moradi, M., & Kadivar, M. (2020) · Journal of Applied Microbiology · doi:10.1111/jam.14984 · Cited by 6 · see citing works
Choi, S. Y., Ko, E. J., Seok, J., Han, H. S., Yoo, K. H., Song, M., Song, K., & Kim, B. J. (2024) · Frontiers in Nutrition · doi:10.3389/fnut.2024.1447863 · Cited by 6 · see citing works
Lee, S. Y., Sekhon, S. S., Kim, H. C., Won, K., Ahn, J., Lee, K., & Kim, Y. (2017) · Toxicology and Environmental Health Sciences · doi:10.1007/s13530-017-0332-2 · Cited by 5 · see citing works
Self-citationProtective effects of oyster polypeptide on cyclophosphamide‐induced immunosuppressed rats
He, Y., Nong, Y., Qin, J., Feng, L., Qin, J., Wang, Q., Deng, L., Tang, S., Zhang, M., Fan, X., et al. (2024) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.13537 · Cited by 4 · see citing works
Autolysis and Cell Death Is Affected by pH in L. reuteri DSM 20016 Cells
Zimmerman, T., & Ibrahim, S. A. (2021) · Foods · doi:10.3390/foods10051026 · Cited by 4 · see citing works
Gut Microbiota and Aging: Targets and Anti-aging Interventions
Singh, B., Catanzaro, R., Mal, G., Gautam, S., Mohania, He, F., Yadav, H., Bissi, L., & Marotta, F. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.62181-5 · Cited by 4 · see citing works
Mechanism of Bacillus coagulans T242 in prevention of Salmonella infection in mice
Gao, X., Yu, J., Lei, C., Jiang, S., Mu, G., & Qian, F. (2024) · Food Bioscience · doi:10.1016/j.fbio.2024.104226 · Cited by 4 · see citing works
Effect of food ingredients on susceptible gut indigenous bacteria
Kuda, T., & Brandelli, A. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85170-1.00022-1 · Cited by 3 · see citing works
Management of asthma using probiotics
Garg, A. P., Ateeq, A., Bisht, N., & Patil, B. (2024) · doi:10.37349/eaa.2024.00026 · Cited by 3 · see citing works
Targeting the Gut Microbiota with Pro- and Postbiotics: Emerging Strategies against Alopecia
Singh, V. B., Hussain, M. S., Das, J., Chellappan, D. K., Chaudhary, P., Sridhar, S. B., Panigrahy, U. P., Ramzan, M., Mondal, M., & Ashique, S. (2026) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-026-10918-x · Cited by 2 · see citing works
PROBIOTIC PROPERTIES OF LACTOBACILLUS REUTERI (L. REUTERI) STRAINS
Novikova, V. P., & Магомедова, Д. М. (2023) · Children s medicine of the North-West · doi:10.56871/cmn-w.2023.75.34.002 · Cited by 3 · see citing works
Diehl, C. (2019) · Ukrainian Journal of Dermatology Venerology Cosmetology · doi:10.30978/ujdvk2019-2-99 · Cited by 2 · see citing works
Knysh, O. V., Pogorila, M. S., & Voyda, Y. V. (2020) · Regulatory Mechanisms in Biosystems · doi:10.15421/022013 · Cited by 2 · see citing works
Probiotics for Atopic Dermatitis: An Update
Kakade, P., Wairkar, S., Lohakare, S., Shah, P., & Patravale, V. B. (2021) · Springer eBooks · doi:10.1007/978-981-16-5628-6_9 · Cited by 2 · see citing works
Bacillus strains prevent lipopolysaccharide-induced inflammation in gut and blood of male mice
Pesarico, A. P., Jesus, G. F. A., Córneo, E. D. S., Borges, H. D. M., Calixto, K. V., Garcez, M. L., Bellettini‐Santos, T., Voytena, A. P. L., Rossetto, M. P., Ramlov, F., et al. (2022) · Journal of Applied Microbiology · doi:10.1093/jambio/lxac021 · Cited by 2 · see citing works
Lactiplantibacillus plantarum ZJUIDS51 improves androgenic alopecia via gut-skin axis
Fu, J., He, Y., Qiao, L., Wu, Z., Wei, Y., Hau, E. H., Xiao, Y., & Ren, D. (2026) · Food Research International · doi:10.1016/j.foodres.2026.118793 · Cited by 1 · see citing works
Uddin, M., Uddin, S., Deb, B., Hussain, T., Rafi, S., & Islam, A. K. M. M. (2024) · International Journal of Gastroenterology · doi:10.11648/j.ijg.20240801.14 · Cited by 2 · see citing works
Immune enhancing effects of Weissella cibaria JW15 in C57BL/6J mice aged 28 months
Park, H.-E., Ahn, H.-S., & Lee, W.-K. (2016) · Journal of Biomedical Translational Research · doi:10.12729/jbtr.2016.17.4.102
Kimoto‐Nira, H. (2018) · Japanese Journal of Lactic Acid Bacteria · doi:10.4109/jslab.29.69
- Authors
- Lee, J., Yang, W., Hostetler, A., Schultz, N., Suckow, M. A., Stewart, K. L., Kim, D. D., & Kim, H. S.
- Affiliations
- University of Notre Dame (US)
- Corresponding author
- Lee, Joon
- Kim, Hyung Soo
- Venue
- BMC Microbiology
- Published
- 2016-04-19
- Volume
- 16
- Issue
- 1
- Pages
- 69-69
- ISSN
- 1471-2180 (ISSN-L)
- PMC
- PMC4837529
- OpenAlex
- W2339853403
- Cited by
- 107
- References
- 53
- Citations by year
- 2026: 4 · 2025: 10 · 2024: 17 · 2023: 9 · 2022: 12 · 2021: 15 · 2020: 8 · 2019: 13 · 2018: 12 · 2017: 5 · 2016: 2
- FWCI
- 13.43
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Microbiology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- California Institute of Technology
- University of Notre Dame
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
- Keywords
- Lactobacillus reuteri, probiotics, anti-inflammatory activity, lactic acid bacteria, TNF-α, THP-1 cells, gut microbiota, aging, sex differences, testosterone, skin health, insulin, immunomodulation
- MeSH terms
- Gastrointestinal Microbiome, Aging, Animals, Anti-Inflammatory Agents, Cell Line, Culture Media, Female, Humans, Male, Mice, Inbred C57BL, Sex Factors, Tumor Necrosis Factor-alpha, Up-Regulation, Probiotics, Mice, Limosilactobacillus reuteri
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