Tauroursodeoxycholic acid reduces glial cell activation in an animal model of acute neuroinflammation
Open accessAbstract
BACKGROUND: Bile acids are steroid acids found predominantly in the bile of mammals. The bile acid conjugate tauroursodeoxycholic acid (TUDCA) is a neuroprotective agent in different animal models of stroke and neurological diseases. However, the anti-inflammatory properties of TUDCA in the central nervous system (CNS) remain unknown. METHODS: The acute neuroinflammation model of intracerebroventricular (icv) injection with bacterial lipopolysaccharide (LPS) in C57BL/6 adult mice was used herein. Immunoreactivity against Iba-1, GFAP, and VCAM-1 was measured in coronal sections in the mice hippocampus. Primary cultures of microglial cells and astrocytes were obtained from neonatal Wistar rats. Glial cells were treated with proinflammatory stimuli to determine the effect of TUDCA on nitrite production and activation of inducible enzyme nitric oxide synthase (iNOS) and NFκB luciferase reporters. We studied the effect of TUDCA on transcriptional induction of iNOS and monocyte chemotactic protein-1 (MCP-1) mRNA as well as induction of protein expression and phosphorylation of different proteins from the NFκB pathway. RESULTS: TUDCA specifically reduces microglial reactivity in the hippocampus of mice treated by icv injection of LPS. TUDCA treatment reduced the production of nitrites by microglial cells and astrocytes induced by proinflammatory stimuli that led to transcriptional and translational diminution of the iNOS. This effect might be due to inhibition of the NFκB pathway, activated by proinflammatory stimuli. TUDCA decreased in vitro microglial migration induced by both IFN-γ and astrocytes treated with LPS plus IFN-γ. TUDCA inhibition of MCP-1 expression induced by proinflammatory stimuli could be in part responsible for this effect. VCAM-1 inmunoreactivity in the hippocampus of animals treated by icv LPS was reduced by TUDCA treatment, compared to animals treated with LPS alone. CONCLUSIONS: We show a triple anti-inflammatory effect of TUDCA on glial cells: i) reduced glial cell activation, ii) reduced microglial cell migratory capacity, and iii) reduced expression of chemoattractants (e.g., MCP-1) and vascular adhesion proteins (e.g., VCAM-1) required for microglial migration and blood monocyte invasion to the CNS inflammation site. Our results present a novel TUDCA anti-inflammatory mechanism, with therapeutic implications for inflammatory CNS diseases.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
TUDCA is effective in attenuating microglial reactivity in LPS-treated mice.
“In addition, TUDCA is effective in attenuating microglial reactivity in LPS-treated mice.367,370,371”
From Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases (2024) · cites this paper as [370]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids
Green, L. C., Wagner, D. A., Glogowski, J. A., Skipper, P. L., Wishnok, J. S., & Tannenbaum, S. R. (1982) · Analytical Biochemistry · doi:10.1016/0003-2697(82)90118-x · Cited by 12,061 · see citing works
Pathobiology of ischaemic stroke: an integrated view
Dirnagl, U., Iadecola, C., & Moskowitz, M. A. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01401-0 · Cited by 3,943 · see citing works
Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue
Mccarthy, K., & de Vellis, J. (1980) · Journal of Cell Biology · doi:10.1083/jcb.85.3.890 · Cited by 3,915 · see citing works
mouse brain in stereotaxic coordinates
Franklin, K. B. J., & Paxinos, G. (1997) · Cited by 3,258 · see citing works
Toll-like Receptor-4 Mediates Lipopolysaccharide-induced Signal Transduction
Chow, J. C., Young, D. W., Golenbock, D. T., Christ, W. J., & Gusovsky, F. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.16.10689 · Cited by 1,924 · see citing works
MCGEER, P., & MCGEER, E. (1995) · Brain Research Reviews · doi:10.1016/0165-0173(95)00011-9 · Cited by 1,287 · see citing works
Dong, Y., & Benveniste, E. N. (2001) · Glia · doi:10.1002/glia.1107 · Cited by 1,286 · see citing works
Aloisi, F. (2001) · Glia · doi:10.1002/glia.1106 · Cited by 1,281 · see citing works
The role of inflammation in CNS injury and disease
Lucas, S., Rothwell, N. J., & Gibson, R. M. (2006) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706400 · Cited by 1,272 · see citing works
Inflammation in Neurodegenerative Disease—A Double-Edged Sword
Wyss-Coray, T., & Mucke, L. (2002) · Neuron · doi:10.1016/s0896-6273(02)00794-8 · Cited by 1,235 · see citing works
The Blood-Brain Barrier in Brain Homeostasis and Neurological Diseases
Weiss, N., Miller, F., Cazaubon, S., & Couraud, P.-O. (2009) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2008.10.022 · Cited by 731 · see citing works
Inflammatory response in acute traumatic brain injury: a double-edged sword
Morganti-Kossmann, M., Rancan, M., Stahel, P., & Kossmann, T. (2002) · Current Opinion in Critical Care · doi:10.1097/00075198-200204000-00002 · Cited by 702 · see citing works
Deng, J., Lu, P. D., Zhang, Y., Scheuner, D. L., Kaufman, R. J., Sonenberg, N., Harding, H. P., & Ron, D. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.23.10161-10168.2004 · Cited by 645 · see citing works
Post-traumatic inflammation following spinal cord injury
Hausmann, O. N. (2003) · Spinal Cord · doi:10.1038/sj.sc.3101483 · Cited by 611 · see citing works
Ursodiol for the Long-Term Treatment of Primary Biliary Cirrhosis
Poupon, R. E., Poupon, R., & Balkau, B. (1994) · New England Journal of Medicine · doi:10.1056/nejm199405123301903 · Cited by 497 · see citing works
Inflammation in central nervous system injury.
Allan, S., & Rothwell, N. (2003) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.2003.1358 · Cited by 336 · see citing works
Keene, C. D., Rodrigues, C. M. P., Eich, T., Chhabra, M. S., Steer, C. J., & Low, W. C. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.162362299 · Cited by 306 · see citing works
The Neuropathological and Behavioral Consequences of Intraspinal Microglial/Macrophage Activation
Popovich, P. G., Guan, Z., McGaughy, V. M., Fisher, L. C., Hickey, W. F., & Basso, D. M. (2002) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/61.7.623 · Cited by 295 · see citing works
PKR Stimulates NF-κB Irrespective of Its Kinase Function by Interacting with the IκB Kinase Complex
Bonnet, M., Weil, R., Dam, E., Hovanessian, A. G., & MEURS, E. F. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.13.4532-4542.2000 · Cited by 234 · see citing works
Rodrigues, C. M. P., Solá, S., Nan, Z., Castro, R. E., Ribeiro, P. S., Low, W. C., & Steer, C. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1031632100 · Cited by 210 · see citing works
Neuroprotection by a Bile Acid in an Acute Stroke Model in the Rat
Rodrigues, C. M. P., Spellman, S. R., Solá, S., Grande, A. W., Linehan-Stieers, C., Low, W. C., & Steer, C. J. (2002) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200204000-00010 · Cited by 160 · see citing works
T-Cell Cytokines in Injury-Induced Neural Damage and Repair
Schroeter, M., & Jander, S. (2005) · NeuroMolecular Medicine · doi:10.1385/nmm:7:3:183 · Cited by 89 · see citing works
Inflammation in the nervous system: The human perspective
Bauer, J., Rauschka, H., & Lassmann, H. (2001) · Glia · doi:10.1002/glia.1112 · Cited by 88 · see citing works
PKR Regulates TLR2/TLR4-Dependent Signaling in Murine Alveolar Macrophages
Cabanski, M., Steinmüller, M., Marsh, L. M., Surdziel, E., Seeger, W., & Lohmeyer, J. (2007) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2007-0010oc · Cited by 81 · see citing works
Gaspar, J. M., Martins, A., Cruz, R., Rodrigues, C. M. P., Ambrósio, A. F., & Santiago, A. R. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.053 · Cited by 78 · see citing works
Mecha, M. (2011) · Protocol Exchange · doi:10.1038/protex.2011.218 · Cited by 65 · see citing works
Joo, S. S., Won, T., & Lee, D. I. (2004) · Archives of Pharmacal Research · doi:10.1007/bf02975850 · Cited by 53 · see citing works
Intracerebral regulation of immune responses
Aloisi, F., Ambrosini, E., Cabezas, S. C., Magliozzi, R., & Serafini, B. (2001) · Annals of Medicine · doi:10.3109/07853890108995960 · Cited by 46 · see citing works
Carrigan, S. O., Pink, D., & Stadnyk, A. W. (2007) · Journal of Leukocyte Biology · doi:10.1189/jlb.0806528 · Cited by 44 · see citing works
Tauroursodeoxycholic acid and secondary damage after spinal cord injury in rats
Çolak, A., Kelten, B., Sağmanligil, A., Akdemir, O., Karaoğlan, A., Şahan, E., Çelik, Ö., & Barut, Ş. (2008) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2007.06.002 · Cited by 36 · see citing works
Saura, M., Zaragoza, C., Dı́az-Cazorla, M., Hernández‐Perera, O., Eng, E., Lowenstein, C. J., Pérez‐Sala, D., & Lamas, S. (1998) · Kidney International · doi:10.1046/j.1523-1755.1998.00725.x · Cited by 36 · see citing works
Yin, J., Tu, J., Lin, H.-J., Shi, F., Liu, R.-L., Zhao, C., Coons, S. W., Kuniyoshi, S. M., & Shi, J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012400 · Cited by 32 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Microbiota–gut–brain axis and its therapeutic applications in neurodegenerative diseases
Loh, J. S., Mak, W. Q., Tan, L. K. S., Ng, C. X., Chan, H. H., Yeow, S. H., Foo, J. B., Ong, Y. S., How, C. W., & Khaw, K. Y. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01743-1 · Cited by 1,193 · see citing works
Neuroinflammation in Alzheimer disease
Heneka, M. T., van der Flier, W. M., Jessen, F., Hoozemanns, J., Thal, D. R., Boche, D., Brosseron, F., Teunissen, C., Zetterberg, H., Jacobs, A. H., et al. (2025) · Nature Reviews Immunology · doi:10.1038/s41577-024-01104-7 · Cited by 638 · see citing works
Inflammogenesis of Secondary Spinal Cord Injury
Anwar, M. A., Shehabi, T. S. A., & Eid, A. H. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00098 · Cited by 442 · see citing works
Nam, H. Y., Nam, J. H., Yoon, G., Lee, J., Nam, Y., Kang, H., Cho, H.-J., Kim, J., & Hoe, H. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1308-0 · Cited by 268 · see citing works
Kusaczuk, M. (2019) · Cells · doi:10.3390/cells8121471 · Cited by 244 · see citing works
Yanguas‐Casás, N., Barreda‐Manso, M. A., Nieto‐Sampedro, M., & Romero‐Ramírez, L. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.25742 · Cited by 223 · see citing works
Self-citationInflammatory pathways in Alzheimer’s disease mediated by gut microbiota
Qian, X.-H., Song, X.-X., Liu, X.-L., Chen, S.-D., & Tang, H.-D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101317 · Cited by 153 · see citing works
Metabolomic Profiling of Bile Acids in Clinical and Experimental Samples of Alzheimer’s Disease
Pan, X., Elliott, C. T., McGuinness, B., Passmore, P., Kehoe, P. G., Hölscher, C., McClean, P. L., Graham, S. F., & Green, B. D. (2017) · Metabolites · doi:10.3390/metabo7020028 · Cited by 153 · see citing works
Bile acids: a communication channel in the gut-brain axis
Monteiro-Cardoso, V. F., Corlianò, M., & Singaraja, R. R. (2021) · NeuroMolecular Medicine · doi:10.1007/s12017-020-08625-z · Cited by 145 · see citing works
Role of the intestinal microbiome, intestinal barrier and psychobiotics in depression
Trzeciak, P., & Herbet, M. (2021) · Nutrients · doi:10.3390/nu13030927 · Cited by 139 · see citing works
Park, T., Chen, H., Kevala, K., Lee, J.-W., & Kim, H.-Y. (2016) · Journal of Neuroinflammation · doi:10.1186/s12974-016-0751-z · Cited by 131 · see citing works
Dionísio, P. A., Amaral, J. D., Ribeiro, M. F., Lo, A. C., D'Hooge, R., & Rodrigues, C. M. P. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.08.034 · Cited by 127 · see citing works
Huang, F., Pariante, C. M., & Borsini, A. (2022) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2021.09.021 · Cited by 117 · see citing works
Bile Acids in Neurodegenerative Disorders
Ackerman, H. D., & Gerhard, G. S. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00263 · Cited by 120 · see citing works
Roles of bile acids signaling in neuromodulation under physiological and pathological conditions
Chen, X., Huang, X., Wang, D., Yu, D., Hou, S., Cui, H., & Song, L. (2023) · Cell & Bioscience · doi:10.1186/s13578-023-01053-z · Cited by 120 · see citing works
Yanguas‐Casás, N., Crespo‐Castrillo, A., CEBALLOS, M. L. D., Chowen, J. A., Azcoitia, Í., Arévalo, M., & García‐Segura, L. M. (2017) · Glia · doi:10.1002/glia.23263 · Cited by 116 · see citing works
Self-citationBile acids as key modulators of the brain-Gut-Microbiota axis in alzheimer’s disease
Mulak, A. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-210608 · Cited by 114 · see citing works
Microglia activation in a model of retinal degeneration and TUDCA neuroprotective effects
Noailles, A., Fernández‐Sánchez, L., Lax, P., & Cuenca, N. (2014) · Journal of Neuroinflammation · doi:10.1186/s12974-014-0186-3 · Cited by 100 · see citing works
Li, S., Hua, D., Wang, Q., Yang, L., Wang, X., Luo, A., & Yang, C. (2019) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyz061 · Cited by 91 · see citing works
Hou, Y., Luan, J., Huang, T., Deng, T., Li, X., Xiao, Z., Zhan, J., Luo, D., Hou, Y., Xu, L., et al. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02248-2 · Cited by 77 · see citing works
Wang, C., Yuan, J., Qin, D., Gu, J., Zhao, B., Zhang, L., Zhao, D., Chen, J., Hou, X., Yang, N., et al. (2016) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2016.03.026 · Cited by 72 · see citing works
Cho, J. G., Lee, J. H., Hong, S. H., Lee, H. N., Kim, C. M., Kim, S. Y., Yoon, K. J., Oh, B. J., Kim, J. H., Jung, S. Y., et al. (2014) · Stem Cells · doi:10.1002/stem.1901 · Cited by 66 · see citing works
Kim, S. J., Ko, W.-K., Jo, M.-J., Arai, Y., Choi, H., Kumar, H., Han, I.-B., & Sohn, S. (2018) · Scientific Reports · doi:10.1038/s41598-018-21621-5 · Cited by 59 · see citing works
Cortez, L. M., Campeau, J. L., Norman, G., Kalayil, M., van der Merwe, J., McKenzie, D. I., & Sim, V. L. (2015) · Journal of Virology · doi:10.1128/jvi.01165-15 · Cited by 59 · see citing works
Tauroursodeoxycholic acid (TUDCA) is neuroprotective in a chronic mouse model of Parkinson’s disease
Cuevas, E., Burks, S., Raymick, J., Robinson, B., Gómez-Crisóstomo, N. P., Escudero-Lourdes, C., Lopez, A. G. G., Chigurupati, S., Hanig, J., Ferguson, S. A., et al. (2022) · Nutritional Neuroscience · doi:10.1080/1028415x.2020.1859729 · Cited by 57 · see citing works
Wu, X., Liu, C., Chen, L., Du, Y.-F., Hu, M., Reed, M. N., Long, Y., Suppiramaniam, V., Hong, H., & Tang, S.-S. (2019) · International Immunopharmacology · doi:10.1016/j.intimp.2019.03.065 · Cited by 56 · see citing works
Zhang, L., Zhang, J., Jiang, X., Yang, L., Zhang, Q., Wang, B., Cui, L., & Wang, X. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.12.005 · Cited by 54 · see citing works
Sun, D., Gu, G., Wang, J., Chai, Y., Fan, Y., Yang, M., Xu, X. J., Gao, W., Li, F. R., Yin, D., et al. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00193 · Cited by 53 · see citing works
RetractedHashimoto’s thyroiditis induces neuroinflammation and emotional alterations in euthyroid mice
Cai, Y., Wang, F., Chen, Z.-X., Li, L., Fan, H., Wu, Z., Ge, J., Hu, W., Wang, Q., & Zhu, D.-F. (2018) · Journal of Neuroinflammation · doi:10.1186/s12974-018-1341-z · Cited by 53 · see citing works
Barrera, M., Aguilera, S., Castro, I., González, S., Carvajal, P., Molina, C., Hermoso, M., & González, M.-J. (2018) · Autoimmunity Reviews · doi:10.1016/j.autrev.2018.02.009 · Cited by 42 · see citing works
Connecting the Gut Microbiota and Neurodegenerative Diseases: the Role of Bile Acids
Wang, S., Xu, C., Liu, H., Wei, W., Zhou, X., Qian, H., Zhou, L., Zhang, H., Wu, L. M., Chen, Z., et al. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03340-9 · Cited by 50 · see citing works
Romero‐Ramírez, L., & Mey, J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25179279 · Cited by 49 · see citing works
Self-citationMicroglia and gut microbiota: A double-edged sword in Alzheimer's disease
Bano, N., Khan, S., Ahamad, S., Kanshana, J. S., Dar, N. J., Khan, S. J., Nazir, A., & Bhat, S. A. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102515 · Cited by 49 · see citing works
The gut-brain axis in ischemic stroke: its relevance in pathology and as a therapeutic target
Benakis, C., & Liesz, A. (2022) · Neurological Research and Practice · doi:10.1186/s42466-022-00222-8 · Cited by 48 · see citing works
Bile acids attenuate PKM2 pathway activation in proinflammatory microglia
Romero-Ramírez, L., García-Rama, C., Wu, S., & Mey, J. (2022) · Scientific Reports · doi:10.1038/s41598-022-05408-3 · Cited by 41 · see citing works
Self-citationNatural Compounds from Saffron and Bear Bile Prevent Vision Loss and Retinal Degeneration
Fernández‐Sánchez, L., Lax, P., Noailles, A., Jeréz, A. A., Maneu, V., & Cuenca, N. (2015) · Molecules · doi:10.3390/molecules200813875 · Cited by 44 · see citing works
Castro, I., Albornoz, N., Aguilera, S., Barrera, M., González, S., Núñez, M., Carvajal, P., Jara, D., Lagos, C., Molina, C., et al. (2019) · Lara D. Veeken · doi:10.1093/rheumatology/kez316 · Cited by 41 · see citing works
Gronbeck, K. R., Rodrigues, C. M. P., Mahmoudi, J., Bershad, E. M., Ling, G. S. F., Bachour, S. P., & Divani, A. A. (2016) · Neurocritical Care · doi:10.1007/s12028-015-0225-7 · Cited by 37 · see citing works
Gómez‐Vicente, V., Lax, P., Fernández‐Sánchez, L., Rondón, N., Esquiva, G., Germaín, F., de la Villa, P., & Cuenca, N. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137826 · Cited by 36 · see citing works
A New Drug Delivery System Based on Tauroursodeoxycholic Acid and PEDOT
Carli, S., Fioravanti, G., Armirotti, A., Ciarpella, F., Prato, M., Ottonello, G., Salerno, M., Scarpellini, A., Perrone, D., Marchesi, E., et al. (2018) · Chemistry - A European Journal · doi:10.1002/chem.201805285 · Cited by 36 · see citing works
Zhu, H., Wang, G., Bai, Y., Tao, Y., Wang, L., Liu, Y., Wu, H., Huang, F., Shi, H., & Wu, X. (2022) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2022.115063 · Cited by 37 · see citing works
Yanguas‐Casás, N., Barreda-Manso, M. A., Pérez-Rial, S., Nieto‐Sampedro, M., & Romero‐Ramírez, L. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0142-6 · Cited by 36 · see citing works
Self-citationStanimirov, B., Đanić, M., Pavlović, N., Zaklan, D., Lazarević, S., Mikov, M., & Stankov, K. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262412167 · Cited by 37 · see citing works
Ellagic Acid Inhibits Neuroinflammation and Cognitive Impairment Induced by Lipopolysaccharides
Dornelles, G. L., de Oliveira, J. S., de Almeida, E. J. R., Mello, C. B. E., Rodrigues, B. R. E., da Silva, C. B., Petry, L. D. S., Pillat, M. M., Palma, T. V., & de Andrade, C. M. (2020) · Neurochemical Research · doi:10.1007/s11064-020-03105-z · Cited by 33 · see citing works
Linking Nonalcoholic Fatty Liver Disease and Brain Disease: Focusing on Bile Acid Signaling
Ren, Z., Li, C.-X., Ma, C., Chen, D., Chen, J., Xu, W., Chen, C.-A., Cheng, F., & Wang, X. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113045 · Cited by 32 · see citing works
Mendes, M. O., Rosa, A. I., Carvalho, A. N., Nunes, M. J., Dionísio, P., Rodrigues, E., Costa, D., Duarte-Silva, S., Maciel, P., Rodrigues, C. M. P., et al. (2019) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2019.01.003 · Cited by 31 · see citing works
Impairment of Hepcidin Upregulation by Lipopolysaccharide in the Interleukin-6 Knockout Mouse Brain
Zhang, F., Hou, H., Yin, Z., Chang, L. Y., Li, F., Chen, Y.-J., Ke, Y., & Qian, Z. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00367 · Cited by 30 · see citing works
Fan, X., Liu, B., Zhou, J., Gu, X., Zhou, Y., Yang, Y., Guo, F., Wei, X., Wang, H., Si, N., et al. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.658376 · Cited by 30 · see citing works
Gut microbiota–astrocyte axis: new insights into age-related cognitive decline
Zhang, L., Wei, J., Liu, X., Li, D., Pang, X., Chen, F., Cao, H., & Lei, P. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-23-01776 · Cited by 28 · see citing works
Beck‐Schimmer, B., Baumann, L., Restin, T., Eugster, P., Hasler, M., Booy, C., & Schläpfer, M. (2017) · European Journal of Anaesthesiology · doi:10.1097/eja.0000000000000668 · Cited by 26 · see citing works
Interorgan communication with the liver: novel mechanisms and therapeutic targets
Zhao, J., Zhang, X., Li, Y., Yu, J., Chen, Z., Niu, Y., Ran, S., Wang, S., Ye, W., Luo, Z., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1314123 · Cited by 28 · see citing works
Zhang, Z., Chen, J., Chen, F., Yu, D., Li, R., Lv, C., Wang, H., Li, H., Li, J., & Cai, Y. (2017) · Cell Stress and Chaperones · doi:10.1007/s12192-017-0862-1 · Cited by 25 · see citing works
Zhang, L., Jiang, X., Zhang, J., Gao, H., Yang, L., Li, D., Zhang, Q., Wang, B., Cui, L., & Wang, X. (2021) · International Immunopharmacology · doi:10.1016/j.intimp.2021.107986 · Cited by 24 · see citing works
Wu, S., Romero‐Ramírez, L., & Mey, J. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.30619 · Cited by 22 · see citing works
Self-citationZhou, R., He, M. X., Fan, J., Li, R., Zuo, Y.-F., Li, B., Gao, G., & Sun, T. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.947295 · Cited by 23 · see citing works
Darmanto, A. G., Yen, T., Jan, J., Linh, T. T. D., Taliyan, R., Yang, C. H., & Sheu, J. (2024) · Pharmacological Research · doi:10.1016/j.phrs.2024.107564 · Cited by 21 · see citing works
Huang, L., Xu, G., Zhang, R., Wang, Y., Ji, J., Long, F., & Sun, Y. (2022) · Lipids in Health and Disease · doi:10.1186/s12944-021-01620-8 · Cited by 20 · see citing works
Gut microbiota in ischemic stroke: Where we stand and challenges ahead
Long, J.-X., Wang, J., Li, Y., & Chen, D. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.1008514 · Cited by 20 · see citing works
Dong, W., Huang, Y., Shu, Y., Fan, X., Tian, X., Yan, Y., Mi, J., Lu, L., Zeng, X., & Cao, Y. (2023) · Food & Function · doi:10.1039/d3fo02651e · Cited by 20 · see citing works
Tung, T.-H., Chen, Y., Lin, Y., & Huang, S. (2022) · Biomedicines · doi:10.3390/biomedicines10071594 · Cited by 19 · see citing works
Gastrointestinal Dysfunction in Stroke
Yong, H. Y. F., Ganesh, A., & Camara-Lemarroy, C. R. (2023) · Seminars in Neurology · doi:10.1055/s-0043-1771470 · Cited by 18 · see citing works
Liu, X., Zhu, B., Zou, H., Hu, D., Gu, Q., Liu, K., & Xu, X. (2015) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-015-2969-3 · Cited by 18 · see citing works
Jo, F., Jo, H., Hilzendeger, A. M., Thompson, A. P., Cassell, M. D., Rutkowski, D. T., Davisson, R. L., Grobe, J. L., & Sigmund, C. D. (2015) · Hypertension · doi:10.1161/hypertensionaha.115.05377 · Cited by 17 · see citing works
Xu, K., Zheng, S., Zhai, Y., Guo, L., Tang, P., Yan, J., Wu, D., & Li, H. (2015) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2015.03.072 · Cited by 17 · see citing works
New oleyl glycoside as anti-cancer agent that targets on neutral sphingomyelinase
Romero‐Ramírez, L., García‐Álvarez, I., Casas, J., Barreda-Manso, M. A., Yanguas‐Casás, N., Nieto‐Sampedro, M., & Fernández‐Mayoralas, A. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2015.07.009 · Cited by 17 · see citing works
Self-citationKim, B., Arai, Y., Choi, B., Park, S., Ahn, J., Han, I., & Lee, S. (2017) · Journal of Industrial and Engineering Chemistry · doi:10.1016/j.jiec.2017.12.027 · Cited by 17 · see citing works
Wu, S., García‐Rama, C., Romero‐Ramírez, L., de Munter, J., Wolters, E. C., Kramer, B. W. W., & Mey, J. (2022) · Biomedicines · doi:10.3390/biomedicines10071501 · Cited by 15 · see citing works
Self-citationTauroursodeoxycholic acid: more than just a neuroprotective bile conjugate
Romero‐Ramírez, L., Nieto‐Sampedro, M., & Yanguas‐Casás, N. (2017) · Neural Regeneration Research · doi:10.4103/1673-5374.198979 · Cited by 15 · see citing works
Self-citationSui, K., Tveter, K. M., Bawagan, F. G., Buckendahl, P., Martinez, S. A., Jaffri, Z. H., MacDonell, A. T., Wu, Y., Duran, R. M., Shapses, S. A., et al. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.900667 · Cited by 15 · see citing works
Mohamed, N. A., Ithmil, M. T., Elkady, A. I., & Salam, S. A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25136922 · Cited by 16 · see citing works
Chandra, S., & Vassar, R. J. (2024) · Immunological Reviews · doi:10.1111/imr.13412 · Cited by 14 · see citing works
Kim, K.-W., Yoon, C., Park, S., Bae, G., Kim, D., Kim, Y., & Oh, H. (2021) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2021/5901653 · Cited by 15 · see citing works
Zhang, Q., Liu, Y., Tang, R., Kong, S., Lv, D., Li, H., Yang, H., & Lin, L. (2024) · Carbohydrate Polymer Technologies and Applications · doi:10.1016/j.carpta.2024.100567 · Cited by 12 · see citing works
Effect of Tauroursodeoxycholic Acid on Inflammation after Ocular Alkali Burn
Huang, Y., Lin, L., Yang, Y., Duan, F., Yuan, M., Lou, B., & Lin, X. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911717 · Cited by 12 · see citing works
Yanguas‐Casás, N., Ojalvo‐Sanz, A. C., Martínez-Vázquez, A., Goneau, M.-F., Gilbert, M., Nieto‐Sampedro, M., & Romero‐Ramírez, L. (2019) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2019.114627 · Cited by 10 · see citing works
Self-citationThe Metabolomic Mind: Microbial Metabolite Programming of Microglia
Verosky, B. G., Bailey, M. T., & Gur, T. (2025) · NeuroImmunoModulation · doi:10.1159/000545484 · Cited by 9 · see citing works
Zhang, Y., Li, J., Li, J., Wang, Y., Cui, M., Li, W., Chen, X., & Jiang, Y. (2025) · GeroScience · doi:10.1007/s11357-025-01790-8 · Cited by 9 · see citing works
Is TGR5 a therapeutic target for the treatment of spinal cord injury?
Smaling, A., Romero‐Ramírez, L., & Mey, J. (2022) · Journal of Neurochemistry · doi:10.1111/jnc.15727 · Cited by 9 · see citing works
Self-citationIdentification of the expression of farnesoid X receptor in astrocytes
He, H., Chen, Z., Chen, D., Lu, X., Huang, C., & Chen, J. (2021) · Neuroreport · doi:10.1097/wnr.0000000000001717 · Cited by 9 · see citing works
Gu, Y., Wang, M., & Mao, Y. (2026) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2026.101247 · Cited by 8 · see citing works
Relationship Between Multiple Sclerosis, Gut Dysbiosis, and Inflammation
Jank, L., & Bhargava, P. (2023) · Neurologic Clinics · doi:10.1016/j.ncl.2023.07.005 · Cited by 8 · see citing works
Li, P.-S., Wang, J., Hao, H., Chen, X., He, X., & Shao, Q. (2025) · Drug Design Development and Therapy · doi:10.2147/dddt.s557300 · Cited by 6 · see citing works
Romero‐Ramírez, L., García‐Rama, C., & Mey, J. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-03963-6 · Cited by 5 · see citing works
Self-citationRole of inflammasomes in neuroinflammation after ischemic stroke
Jung, K., & Seong, S. (2021) · encephalitis · doi:10.47936/encephalitis.2021.00073 · Cited by 5 · see citing works
High Dose and Delayed Treatment with Bile Acids Ineffective in RML Prion-Infected Mice
Norman, G., Campeau, J. L., & Sim, V. L. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00222-18 · Cited by 5 · see citing works
Ursodeoxycholic acid alleviates multiple sclerosis via TGR5-dependent microglial regulation in mice
Sonoda, Y., Aizawa, F., Tomochika, N., Miyauchi, K., Nishibashi, A., Takahashi, S., Kosako, H., Tanida, S., Yagi, K., Niimura, T., et al. (2025) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2025.177941 · Cited by 4 · see citing works
Atlıhan, Y. S., Öztüzün, A., Tuzcu, H., Kırımlıoğlu, E., Başsorgun, C. İ., Doğan, M. E., & Aslan, M. (2025) · Cell Biology International · doi:10.1002/cbin.70084 · Cited by 4 · see citing works
Xu, K., Zheng, S., Guo, L., Li, S., Wang, L., Tang, P., Yan, J., Wu, D., & Li, H. (2015) · RSC Advances · doi:10.1039/c5ra18985c · Cited by 3 · see citing works
Singh, G., & Aran, K. R. (2026) · Biogerontology · doi:10.1007/s10522-025-10384-y · Cited by 2 · see citing works
Fan, Q., Takarada-Iemata, M., Tanaka, T., Nguyen, L. D., Okitani, N., Yang, R.-R., Tamatani, T., Ishii, H., Hattori, T., Kidoya, H., et al. (2026) · Cell Death and Disease · doi:10.1038/s41419-026-08461-2 · Cited by 2 · see citing works
Zhang, N., Li, Y., Zhang, X., Chrenek, M. A., Wang, J., Girardot, P. E., Sellers, J. T., Geisert, E. E., Nickerson, J. M., & Boatright, J. H. (2025) · Pharmaceuticals · doi:10.3390/ph18040569 · Cited by 1 · see citing works
Du, X., Li, S., Wu, G., Cai, H., Sun, C.-Y., Lin, H., Cai, Y.-F., & Wang, Q. (2026) · Rejuvenation Research · doi:10.1177/15491684251409076 · Cited by 1 · see citing works
Update Review of the Relationship Between Gut Microbiota and Neurodegenerative Diseases
Wang, Y., Jing, G., Fu, Y., Li, Y., & Wu, C. (2024) · Diseases & Research · doi:10.54457/dr.202401007 · Cited by 1 · see citing works
Using TUDCA to treat Alzheimer's disease after pathology onset in APP/PS1 mice
Dionísio, P. (2014) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Using TUDCA to treat Alzheimer's disease after pathology onset in APP/PS1 mice
Farmácia, F. D. (2014)
Mendes, M. O., Rosa, A. I., Carvalho, A. N., Nunes, M. J., Dionísio, P. A., Rodrigues, E., Costa, D., Duarte‐Silva, S., Maciel, P., Rodrigues, C. M. P., et al. (2021) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2021.103626
C-64 進行非小細胞癌に対するCDDP+VDS+MMC療法とCDDP+VDS+IFX療法の検討
西, 耕., 中積, 泰., 水島, 豊., 中村, 裕., 山之内, 菊., 斉藤, 元., 藤村, 政., 岡藤, 和., 飴嶋, 慎., & 金森, 一. (1992) · 肺癌
Study on the Association between Bile Acid Levels and Prognostic Factors of Ischemic Stroke
霍, 燕. (2022) · Advances in Clinical Medicine · doi:10.12677/acm.2022.126730
Gut–brain communication through microbes
Green, M., & Foster, J. A. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-90144-4.00002-1
Hou, Y., Luan, J., Huang, T., Deng, T., Li, X., Xiao, Z., Zhan, J., Luo, D., Hou, Y., Xu, L., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16650125
- Authors
- Yanguas-Casás, N., Barreda-Manso, M. A., Nieto-Sampedro, M., & Romero-Ramírez, L.
- Affiliations
- Instituto Cajal (ES)
- Venue
- Journal of Neuroinflammation
- Published
- 2014-03-19
- Volume
- 11
- Issue
- 1
- Pages
- 50-50
- ISSN
- 1742-2094 (ISSN-L)
- PMC
- PMC4000131
- OpenAlex
- W2119521536
- Cited by
- 103
- References
- 33
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 12 · 2023: 6 · 2022: 13 · 2021: 13 · 2020: 3 · 2019: 7 · 2018: 6 · 2017: 8 · 2016: 7 · 2015: 8 · 2014: 5
- FWCI
- 4.86
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Journal of Neuroinflammation (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
- Funders
- Ministerio de Ciencia e Innovación (SAF2009-11257, SAF2012-40126)
- Topics
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Keywords
- tauroursodeoxycholic acid, bile acids, neuroinflammation, glial activation, microglial activation, astrocytes, lipopolysaccharide, NF-κB signaling, nitric oxide synthase, MCP-1, VCAM-1, microglial migration, hippocampus, anti-inflammatory activity, neuroprotection, blood-brain barrier
- MeSH terms
- Animals, Animals, Newborn, Calcium-Binding Proteins, Cell Movement, Cells, Cultured, Cholagogues and Choleretics, Disease Models, Animal, Encephalitis, Gene Expression Regulation, Glial Fibrillary Acidic Protein, Hippocampus, Injections, Intraventricular, Lipopolysaccharides, Mice, Inbred C57BL, Microfilament Proteins, Neuroglia, Nitrites, Taurochenodeoxycholic Acid, Rats, Wistar, Vascular Cell Adhesion Molecule-1, Cell Proliferation
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
