Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats
Abstract
Background and aims Intestinal barrier impairment is incriminated in the pathophysiology of intestinal gut disorders associated with psychiatric comorbidity. Increased intestinal permeability associated with upload of lipopolysaccharides (LPS) translocation induces depressive symptoms. Gut microbiota and probiotics alter behavior and brain neurochemistry. Since Lactobacillus farciminis suppresses stress-induced hyperpermeability, we examined whether (i) L. farciminis affects the HPA axis stress response, (ii) stress induces changes in LPS translocation and central cytokine expression which may be reversed by L. farciminis, (iii) the prevention of "leaky" gut and LPS upload are involved in these effects.Methods At the end of the following treatments female rats were submitted to a partial restraint stress (PRS) or sham-PRS: (i) oral administration of L. farciminis during 2 weeks, (ii) intraperitoneal administration of ML-7 (a specific myosin light chain kinase inhibitor), (iii) antibiotic administration in drinking water during 12 days. After PRS or sham-PRS session, we evaluated LPS levels in portal blood, plasma corticosterone and adrenocorticotropic hormone (ACTH) levels, hypothalamic corticotropin releasing factor (CRF) and pro-inflammatory cytokine mRNA expression, and colonic paracellular permeability (CPP).Results PRS increased plasma ACTH and corticosterone; hypothalamic CRF and pro-inflammatory cytokine expression; CPP and portal blood concentration of LPS. L. farciminis and ML-7 suppressed stress-induced hyperpermeability, endotoxemia and prevented HPA axis stress response and neuroinflammation. Antibiotic reduction of luminal LPS concentration prevented HPA axis stress response and increased hypothalamic expression of pro-inflammatory cytokines.Conclusion The attenuation of the HPA axis response to stress by L. farciminis depends upon the prevention of intestinal barrier impairment and decrease of circulating LPS levels.
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A connection has been established between the digestive tract and stress.
“Moreover, a connection has been established between the digestive tract and stress [291, 292].”
From International Society of Sports Nutrition Position Stand: Probiotics (2019) · cites this paper as [291]
Lactobacillus helveticus reduces plasma ACTH and corticosterone concentrations in response to stress in rats and can restore hippocampal serotonin (5-HT) and NE levels.
“Lactobacillus helveticus also reduces anxiety [133] and plasma ACTH and corticosterone concentrations in response to stress in rats and can restore hippocampal serotonin (5-HT) and NE levels [74].”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [167]
Lactobacillus farciminis and Lactobacillus helveticus NS8 have been shown to decrease plasma ACTH and corticosterone concentrations in response to stress in rats, as well as restore hippocampal serotonin and NE levels and decrease neuroinflammation.
“Lactobacillus farciminis and Lactobacillus helveticus NS8 have been shown to decrease plasma ACTH and corticosterone concentrations in response to stress in rats [167, 168], as well as restore hippocampal serotonin and NE levels and decrease neuroinflammation [169].”
From Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes (2016) · cites this paper as [167]
Pre-treatment with L. farciminis reduced HPA hyper-reactivity, intestinal permeability, and neuroinflammation resulting from restraint stress.
“Similarly, pre-treatment with L. farciminis reduced HPA hyper-reactivity, intestinal permeability, and neuroinflammation resulting from restraint stress (367).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [367]
Various studies have reported beneficial effects of probiotics by enhancing intestinal epithelial integrity, protecting from barrier disruption, stimulating a healthy homeostasis of the mucosal immune system and suppressing pathogenic bacterial growth.
“Various studies have reported the beneficial effects of probiotics by enhancing intestinal epithelial integrity, protecting from barrier disruption, stimulating a healthy homeostasis of the mucosal immune system and suppressing pathogenic bacterial growth (Ait-Belgnaoui et al., 2012;Corridoni et al., 2012;Patel et al., 2012;Sartor, 2005;Zareie et al., 2006).”
From The Gut-Brain Axis in Parkinson’s Disease: Possibilities for Food-Based Therapies (2017) · cites this paper as Ait-Belgnaoui et al., 2012
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Cani, P. D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A. M., Delzenne, N. M., & Burcelin, R. (2008) · Diabetes · doi:10.2337/db07-1403 · Cited by 4,819 · see citing works
Intestinal mucosal barrier function in health and disease
Turner, J. R. (2009) · Nature reviews. Immunology · doi:10.1038/nri2653 · Cited by 3,952 · see citing works
Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data
Ruijter, J. M., Ramakers, C., Hoogaars, W. M. H., Karlen, Y., Bakker, O., van den Hoff, M. J. B., & Moorman, A. F. M. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp045 · Cited by 3,043 · see citing works
Sudo, N., Chida, Y., Aiba, Y., Sonoda, J., Oyama, N., Yu, X., Kubo, C., & Koga, Y. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063388 · Cited by 2,735 · see citing works
Swanson, L. W., Sawchenko, P. E., Rivier, J., & Vale, W. W. (2008) · Neuroendocrinology · doi:10.1159/000123454 · Cited by 1,953 · see citing works
The rat brain in stereotaxic coordinates (2nd edn)
Herman, J. P., & Watson, S. J. (1987) · Trends in Neurosciences · doi:10.1016/0166-2236(87)90017-8 · Cited by 1,751 · see citing works
Bercik, P., Denou, E., Collins, J., Jackson, W., Lu, J., Jury, J., Deng, Y., Blennerhassett, P., Macri, J., McCoy, K. D., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.04.052 · Cited by 1,748 · see citing works
Neufeld, K. M., Kang, N., Bienenstock, J., & Foster, J. A. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2010.01620.x · Cited by 1,392 · see citing works
Spiller, R. C., Jenkins, D., Thornley, J. P., Hebden, J. M., Wright, T., Skinner, M., & Neal, K. R. (2000) · Gut · doi:10.1136/gut.47.6.804 · Cited by 1,155 · see citing works
Kassinen, A., Krogius-Kurikka, L., Mäkivuokko, H., Rinttilä, T., Paulin, L., Corander, J., Malinen, E., Apajalahti, J., & Palva, A. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.04.005 · Cited by 1,002 · see citing works
Bacterial infection causes stress-induced memory dysfunction in mice
Gareau, M. G., Wine, E., Rodrigues, D. M., Cho, J. H., Whary, M. T., Philpott, D. J., MacQueen, G., & Sherman, P. M. (2011) · Gut · doi:10.1136/gut.2009.202515 · Cited by 909 · cited 1× · see citing works
“rodentium was not associated with behavioral abnormalities, exposure to an acute stress of previously infected mice during infection or after bacterial clearance is associated with memory dysfunction (Gareau et al., 2011).”
BackgroundMalinen, E., Rinttila, T., Kajander, K., Matto, J., Kassinen, A., Krogius, L., Saarela, M., Korpela, R., & Palva, A. (2005) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2005.40312.x · Cited by 699 · see citing works
Alterations in intestinal permeability
Arrieta, M., Bistritz, L., & Meddings, J. B. (2006) · Gut · doi:10.1136/gut.2005.085373 · Cited by 634 · see citing works
Intestinal permeability and the prediction of relapse in Crohn's disease
Wyatt, J., Vogelsang, H., Hübl, W., Waldhoer, T., & Lochs, H. (1993) · The Lancet · doi:10.1016/0140-6736(93)90882-h · Cited by 626 · see citing works
Maes, M. H. J., Kubera, M., & Leunis, J. (2008) · PubMed · Cited by 607 · see citing works
Frank, M. G., Baratta, M. V., Sprunger, D. B., Watkins, L. R., & Maier, S. F. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2006.03.005 · Cited by 578 · see citing works
Antidepressant-Like Effects of the Histone Deacetylase Inhibitor, Sodium Butyrate, in the Mouse
Schroeder, F. A., Lin, C. L., Crusio, W. E., & Akbarian, S. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.06.036 · Cited by 541 · see citing works
Mittermaier, C., Dejaco, C., Waldhoer, T., Oefferlbauer-Ernst, A., Miehsler, W., Beier, M., Tillinger, W., Gangl, A., & Moser, G. (2004) · Psychosomatic Medicine · doi:10.1097/01.psy.0000106907.24881.f2 · Cited by 532 · see citing works
Gareau, M. G., Jury, J., MacQueen, G., Sherman, P. M., & Perdue, M. H. (2007) · Gut · doi:10.1136/gut.2006.117176 · Cited by 472 · see citing works
Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice
Verdú, E. F., Bercik, P., Verma-Gandhu, M., Huang, X.-X., Blennerhassett, P., Jackson, W., Mao, Y., Wang, L., Rochat, F., & Collins, S. M. (2006) · Gut · doi:10.1136/gut.2005.066100 · Cited by 448 · see citing works
Goehler, L. E., Gaykema, R. P. A., Opitz, N., Reddaway, R., Badr, N., & Lyte, M. (2005) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2004.09.002 · Cited by 442 · see citing works
The Role of the Vagus Nerve in Cytokine‐to‐Brain Communication
Maier, S. F., Goehler, L. E., Fleshner, M., & Watkins, L. R. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09569.x · Cited by 439 · see citing works
Zareie, M., Johnson‐Henry, K. C., Jury, J., Yang, P.-C., Ngan, B., McKay, D. M., Söderholm, J. D., Perdue, M. H., & Sherman, P. M. (2006) · Gut · doi:10.1136/gut.2005.080739 · Cited by 423 · see citing works
Interleukin-1 (IL-1): A central regulator of stress responses
Goshen, I., & Yirmiya, R. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2008.10.001 · Cited by 399 · see citing works
Intestinal membrane permeability and hypersensitivity in the irritable bowel syndrome
Zhou, Q., Zhang, B., & Verne, N. G. (2009) · Pain · doi:10.1016/j.pain.2009.06.017 · Cited by 373 · see citing works
Ek, M., Kurosawa, M., Lundeberg, T., & Ericsson, A. B. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-22-09471.1998 · Cited by 370 · see citing works
Inflammatory bowel disease is associated with changes of enterocytic junctions
Gaßler, N., Rohr, C. M., Schneider, A., Kartenbeck, J., Bach, A., Obermüller, N., Otto, H. F., & Autschbach, F. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.281.1.g216 · Cited by 363 · see citing works
LYTE, M., LI, W., OPITZ, N., GAYKEMA, R., & GOEHLER, L. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.06.019 · Cited by 334 · see citing works
Is small intestinal permeability really increased in relatives of patients with Crohn's disease?
May, G. R., Sutherland, L. R., & Meddings, J. B. (1993) · Gastroenterology · doi:10.1016/0016-5085(93)90638-s · Cited by 316 · see citing works
Mättö, J., Maunuksela, L., Kajander, K., Palva, A., Korpela, R., Kassinen, A., & Saarela, M. (2005) · FEMS Immunology & Medical Microbiology · doi:10.1016/j.femsim.2004.08.009 · Cited by 301 · see citing works
Meddings, J. B., & Swain, M. G. (2000) · Gastroenterology · doi:10.1053/gast.2000.18152 · Cited by 269 · see citing works
Stress-induced changes in intestinal transit in the rat: a model for irritable bowel syndrome.
Williams, C. L., Villar, R., Peterson, J., & Burks, T. F. (1988) · Gastroenterology · doi:10.1016/0016-5085(88)90231-4 · Cited by 248 · see citing works
Ferrier, L., Bérard, F., Debrauwer, L., Chabo, C., Langella, P., Bueno, L. P., & Fioramonti, J. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.050617 · Cited by 247 · see citing works
Self-citationCorticotropin-releasing factor directly mediates colonic responses to stress
Williams, C. L., Peterson, J. M., Villar, R. G., & Burks, T. F. (1987) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1987.253.4.g582 · Cited by 244 · see citing works
Leaky gut and diabetes mellitus: what is the link?
de Kort, S., Keszthelyi, D., & Masclee, A. (2011) · Obesity Reviews · doi:10.1111/j.1467-789x.2010.00845.x · Cited by 233 · see citing works
Acute stressors stimulate ion secretion and increase epithelial permeability in rat intestine
Saunders, P. R., Kosecka, U., McKay, D. M., & Perdue, M. H. (1994) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1994.267.5.g794 · Cited by 215 · see citing works
The structure and regulation of tight junctions
Anderson, J. M., Balda, M. S., & Fanning, A. S. (1993) · Current Opinion in Cell Biology · doi:10.1016/0955-0674(93)90024-k · Cited by 204 · see citing works
Ait-Belgnaoui, A. (2005) · Gut · doi:10.1136/gut.2005.084194 · Cited by 189 · see citing works
Self-citationVerdú, E. F., Bercík, P., Bergonzelli, G. E., Huang, X.-X., Blennerhasset, P., Rochat, F., Fiaux, M., Mansourian, R., Corthésy-Theulaz, I., & Collins, S. M. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.06.007 · Cited by 180 · see citing works
Ait-Belgnaoui, A., Bradesi, S., Fioramonti, J., Theodorou, V., & Bueno, L. (2005) · Pain · doi:10.1016/j.pain.2004.10.002 · Cited by 171 · see citing works
Self-citationStress-induced enhancement of colitis in rats: CRF and arginine vasopressin are not involved
Gué, M., Bonbonne, C., Fioramonti, J., Moré, J., Rio-Lacheze, C. D., Coméra, C., & Bueno, L. P. (1997) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1997.272.1.g84 · Cited by 148 · see citing works
Self-citationLu, P., Zhu, X., Xu, Z.-L., Zhou, Q., Zhang, J., & Wu, F. (2009) · Surgery · doi:10.1016/j.surg.2008.10.010 · Cited by 124 · see citing works
Cholinergic nerves mediate stress-induced intestinal transport abnormalities in Wistar-Kyoto rats
Saunders, P. R., Hanssen, N. P. M., & Perdue, M. H. (1997) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1997.273.2.g486 · Cited by 118 · see citing works
Definition and Classification of Irritable Bowel Syndrome: Current Consensus and Controversies
Longstreth, G. F. (2005) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2005.02.011 · Cited by 95 · see citing works
Wu, X., Guo, R., Chen, P., Wang, Q., & Cunningham, P. N. (2009) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00089.2009 · Cited by 89 · see citing works
Hagan, P., Poole, S., & Bristow, A. F. (1993) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0110031 · Cited by 85 · see citing works
Inhibition of the myosin light chain kinase prevents hypoxia‐induced blood–brain barrier disruption
Kuhlmann, C. R. W., Tamaki, R., Gamerdinger, M., Leßmann, V., Behl, C., Kempski, O. S., & Luhmann, H. J. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04506.x · Cited by 85 · see citing works
Yurdaydın, C., Walsh, T. J., Engler, H. D., Ha, J., Li, Y., Jones, E. A., & Basile, A. S. (1995) · Brain Research · doi:10.1016/0006-8993(95)00241-h · Cited by 82 · see citing works
Eutamène, H., Théodorou, V., Fioramonti, J., & Bueno, L. P. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.052274 · Cited by 78 · see citing works
Self-citationEffect of ischemia on intestinal permeability of lipopolysaccharides
Drewe, J., Beglinger, C., & Fricker, G. (2001) · European Journal of Clinical Investigation · doi:10.1046/j.1365-2362.2001.00792.x · Cited by 77 · see citing works
Hueston, C. M., Barnum, C. J., Eberle-Singh, J. A., Ferraioli, F. J., Buck, H. M., & Terrence Deak, B. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.03.013 · Cited by 65 · see citing works
51CrEDTA colonic permeability and therapy response in patients with ulcerative colitis
Arslan, G., Atasever, T., Cindoruk, M., & Yıldırım, İ. (2001) · Nuclear Medicine Communications · doi:10.1097/00006231-200109000-00009 · Cited by 64 · see citing works
Effects of interleukin-1 infused into brain are antagonized by α-MSH in a dose-dependent manner
Weiss, J. M., Sundar, S. K., Cierpial, M. A., & Ritchie, J. (1991) · European Journal of Pharmacology · doi:10.1016/0014-2999(91)90087-7 · Cited by 52 · see citing works
Lamine, F., Eutamène, H., Fioramonti, J., Bueno, L. P., & Théodorou, V. (2004) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365520410007953 · Cited by 45 · see citing works
Self-citationYamazaki, T., Kimoto, T., Higuchi, K., Ohta, Y., Kawato, S., & Kominami, S. A. J. (1998) · Endocrinology · doi:10.1210/endo.139.12.6338 · Cited by 44 · see citing works
Wadgaonkar, R., Dudek, S. M., Zaiman, A., Linz-McGillem, L. A., Verin, A. D., Nurmukhambetova, S. T., Romer, L. H., & Garcia, J. G. N. (2005) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20472 · Cited by 35 · see citing works
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Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour
Cryan, J. F., & Dinan, T. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3346 · Cited by 4,572 · see citing works
Gut–brain axis: How the microbiome influences anxiety and depression
Foster, J. A., & McVey Neufeld, K.-A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.01.005 · Cited by 2,460 · see citing works
Altered fecal microbiota composition in patients with major depressive disorder
Jiang, H., Ling, Z., Zhang, Y., Mao, H., Ma, Z., Yin, Y., Wang, W., Tang, W., Tan, Z., Shi, J., et al. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.03.016 · Cited by 2,275 · see citing works
Interactions between the microbiota, immune and nervous systems in health and disease
Fung, T. C., Olson, C. A., & Hsiao, E. Y. (2017) · Nature Neuroscience · doi:10.1038/nn.4476 · Cited by 1,900 · see citing works
The central nervous system and the gut microbiome
Sharon, G., Sampson, T. R., Geschwind, D. H., & Mazmanian, S. K. (2016) · Cell · doi:10.1016/j.cell.2016.10.027 · Cited by 1,513 · see citing works
Psychobiotics: A novel class of psychotropic
Dinan, T. G., Stanton, C., & Cryan, J. F. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.05.001 · Cited by 1,287 · see citing works
Stress & the gut-brain axis: Regulation by the microbiome
Foster, J. A., Rinaman, L., & Cryan, J. F. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.03.001 · Cited by 1,150 · see citing works
Kelly, J. R., Kennedy, P. J., Cryan, J. F., Dinan, T. G., Clarke, G., & Hyland, N. P. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00392 · Cited by 1,110 · see citing works
Microbiota and neurodevelopmental windows: implications for brain disorders
Borre, Y. E., O’Keeffe, G. W., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2014) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2014.05.002 · Cited by 1,089 · see citing works
Psychobiotics and the manipulation of bacteria–gut–brain signals
Sarkar, A., Lehto, S. M., Harty, S., Dinan, T. G., Cryan, J. F., & Burnet, P. W. J. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.09.002 · Cited by 1,068 · see citing works
Correlation between the human fecal microbiota and depression
Naseribafrouei, A., Hestad, K., Avershina, E., Sekelja, M., Linløkken, A., Wilson, R., & Rudi, K. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12378 · Cited by 1,044 · see citing works
Leclercq, S., Matamoros, S., Cani, P. D., Neyrinck, A. M., Jamar, F., Stärkel, P., Windey, K., Tremaroli, V., Bäckhed, F., Verbeke, K., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1415174111 · Cited by 972 · see citing works
From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways
Rogers, G. B., Keating, D. J., Young, R. L., Wong, M.-L., Licinio, J., & Wesselingh, S. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.50 · Cited by 969 · see citing works
Inflammation: Depression Fans the Flames and Feasts on the Heat
Kiecolt-Glaser, J. K., Derry, H. M., & Fagundes, C. P. (2015) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2015.15020152 · Cited by 844 · see citing works
The role of microbiome in central nervous system disorders
Wang, Y., & Kasper, L. H. (2014) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.12.015 · Cited by 803 · see citing works
Brain–Gut Interactions in Inflammatory Bowel Disease
Bonaz, B. L., & Bernstein, C. N. (2013) · Gastroenterology · doi:10.1053/j.gastro.2012.10.003 · Cited by 667 · see citing works
Steenbergen, L., Sellaro, R., van Hemert, S., Bosch, J. A., & Colzato, L. S. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2015.04.003 · Cited by 671 · see citing works
Liang, S., Wang, T., Hu, X., Luo, J., Li, W., Wu, X., Duan, Y., & Jin, F. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.033 · Cited by 651 · see citing works
Microbial genes, brain & behaviour – epigenetic regulation of the gut–brain axis
Stilling, R. M., Dinan, T. G., & Cryan, J. F. (2014) · Genes, Brain and Behavior · doi:10.1111/gbb.12109 · Cited by 637 · see citing works
Gut Microbiota’s Effect on Mental Health: The Gut-Brain Axis
Clapp, M., Aurora, N., Herrera, L., Bhatia, M., Wilen, E., & Wakefield, S. (2017) · Clinics and Practice · doi:10.4081/cp.2017.987 · Cited by 608 · see citing works
Petra, A. I., Panagiotidou, S., Hatziagelaki, E., Stewart, J. M., Conti, P., & Theoharides, T. C. (2015) · Clinical Therapeutics · doi:10.1016/j.clinthera.2015.04.002 · Cited by 592 · see citing works
Regulation of the stress response by the gut microbiota: implications for psychoneuroendocrinology
Dinan, T. G., & Cryan, J. F. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.03.007 · Cited by 577 · see citing works
Clark, A., & Mach, N. (2016) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-016-0155-6 · Cited by 583 · see citing works
“Lactobacillus farciminis and Lactobacillus helveticus NS8 have been shown to decrease plasma ACTH and corticosterone concentrations in response to stress in rats [167, 168], as well as restore hippocampal serotonin and NE levels and decrease neuroinflammation [169].”
BackgroundThe microbiome and host behavior
Vuong, H. E., Yano, J. M., Fung, T. C., & Hsiao, E. Y. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031347 · Cited by 537 · see citing works
Schmidt, K., Cowen, P. J., Harmer, C. J., Tzortzis, G., Errington, S., & Burnet, P. W. J. (2015) · Psychopharmacology · doi:10.1007/s00213-014-3810-0 · Cited by 522 · see citing works
The microbiome: a key regulator of stress and neuroinflammation
Rea, K., Dinan, T. G., & Cryan, J. F. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.03.001 · Cited by 508 · see citing works
Feeding the microbiota–gut–brain axis: Diet, microbiome, and neuropsychiatry
Sandhu, K. V., Sherwin, E., Schellekens, H., Stanton, C., Dinan, T. G., & Cryan, J. F. (2017) · Translational Research · doi:10.1016/j.trsl.2016.10.002 · Cited by 491 · see citing works
Gut microbiota and the neuroendocrine system
Farzi, A., Fröhlich, E. E., & Holzer, P. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0600-5 · Cited by 478 · see citing works
The effects of probiotics on depressive symptoms in humans: a systematic review
Wallace, C. J. K., & Milev, R. (2017) · Annals of General Psychiatry · doi:10.1186/s12991-017-0138-2 · Cited by 471 · see citing works
The microbiome: stress, health and disease
Moloney, R. D., Desbonnet, L., Clarke, G., Dinan, T. G., & Cryan, J. F. (2014) · Mammalian Genome · doi:10.1007/s00335-013-9488-5 · Cited by 430 · see citing works
Savignac, H. M., Kiely, B., Dinan, T. G., & Cryan, J. F. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12427 · Cited by 418 · see citing works
Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis
Rusch, J. A., Layden, B. T., & Dugas, L. R. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1130689 · Cited by 415 · see citing works
Gut microbiota in autism and mood disorders
Mangiola, F. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i1.361 · Cited by 413 · see citing works
Relationship between the gut microbiome and brain function
Mohajeri, M. H., La Fata, G., Steinert, R. E., & Weber, P. (2018) · Nutrition Reviews · doi:10.1093/nutrit/nuy009 · Cited by 376 · see citing works
Bifidobacteria modulate cognitive processes in an anxious mouse strain
Savignac, H. M., Tramullas, M., Kiely, B., Dinan, T. G., & Cryan, J. F. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.02.044 · Cited by 365 · see citing works
The HPA axis dysregulation in severe mental illness: Can we shift the blame to gut microbiota?
Misiak, B., Łoniewski, I., Marlicz, W., Frydecka, D., Szulc, A., Rudzki, L., & Samochowiec, J. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109951 · Cited by 343 · see citing works
The gut-brain axis: the missing link in depression
Evrensel, A., & Ceylan, M. E. (2015) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2015.13.3.239 · Cited by 338 · see citing works
Effect of probiotics on central nervous system functions in animals and humans: a systematic review
Wang, H., Lee, I.-S., Braun, C., & Enck, P. (2016) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm16018 · Cited by 334 · see citing works
The Impact of Microbiota on Brain and Behavior: Mechanisms & Therapeutic Potential
Borre, Y. E., Moloney, R. D., Clarke, G., Dinan, T. G., & Cryan, J. F. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-0897-4_17 · Cited by 329 · see citing works
Luna, R. A., & Foster, J. A. (2015) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2014.10.007 · Cited by 325 · see citing works
The role of neuroimmune signaling in alcoholism
Crews, F. T., Lawrimore, C. J., Walter, T. J., & Coleman, L. G. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.01.031 · Cited by 321 · see citing works
Stress induces endotoxemia and low-grade inflammation by increasing barrier permeability
de Punder, K., & Pruimboom, L. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00223 · Cited by 321 · see citing works
Autism spectrum disorders and intestinal microbiota
De Angelis, M., Francavilla, R., Piccolo, M., De Giacomo, A., & Gobbetti, M. (2015) · Gut Microbes · doi:10.1080/19490976.2015.1035855 · Cited by 311 · see citing works
Harshaw, C. (2015) · Psychological Bulletin · doi:10.1037/a0038101 · Cited by 302 · see citing works
Microbiota regulation of the mammalian gut-brain axis
Burokas, A., Moloney, R. D., Dinan, T. G., & Cryan, J. F. (2015) · Advances in applied microbiology · doi:10.1016/bs.aambs.2015.02.001 · Cited by 300 · see citing works
Irritable bowel syndrome: a gut microbiota-related disorder?
Bhattarai, Y., Muniz Pedrogo, D. A., & Kashyap, P. C. (2017) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00338.2016 · Cited by 294 · see citing works
Interplay between the gut-brain axis, obesity and cognitive function
Agustí, A., García-Pardo, M. P., López-Almela, I., Campillo, I., Maes, M., Romaní-Pérez, M., & Sanz, Y. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00155 · Cited by 294 · see citing works
Kato-Kataoka, A., Nishida, K., Takada, M., Kawai, M., Kikuchi-Hayakawa, H., Suda, K., Ishikawa, H., Gondo, Y., Shimizu, K., Matsuki, T., et al. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.04134-15 · Cited by 288 · see citing works
Golubeva, A. V., Crampton, S., Desbonnet, L., Edge, D., O'Sullivan, O., Lomasney, K. W., Zhdanov, A. V., Crispie, F., Moloney, R. D., Borre, Y. E., et al. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.06.002 · Cited by 283 · see citing works
Fermented foods, microbiota, and mental health: ancient practice meets nutritional psychiatry
Selhub, E. M., Logan, A. C., & Bested, A. C. (2014) · Journal of Physiological Anthropology · doi:10.1186/1880-6805-33-2 · Cited by 280 · 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
Unhealthy gut, unhealthy brain: The role of the intestinal microbiota in neurodegenerative diseases
Spielman, L. J., Gibson, D. L., & Klegeris, A. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2018.08.005 · Cited by 266 · see citing works
Luo, Y., Zeng, B., Zeng, L., Du, X., Li, B., Huo, R., Liu, L., Wang, H., Dong, M., Pan, J., et al. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0240-5 · Cited by 245 · see citing works
Microbiome disturbances and autism spectrum disorders
Rosenfeld, C. S. (2015) · Drug Metabolism and Disposition · doi:10.1124/dmd.115.063826 · Cited by 229 · see citing works
The role of the gut microbiota in dietary interventions for depression and anxiety
Bear, T. L. K., Dalziel, J. E., Coad, J., Roy, N. C., Butts, C. A., & Gopal, P. K. (2020) · Advances in Nutrition · doi:10.1093/advances/nmaa016 · Cited by 229 · see citing works
Jang, H.-M., Lee, K.-E., & Kim, D.-H. (2019) · Nutrients · doi:10.3390/nu11040819 · Cited by 208 · see citing works
The Gut-Brain Axis in Parkinson’s Disease: Possibilities for Food-Based Therapies
Perez-Pardo, P., Kliest, T., Dodiya, H. B., Broersen, L. M., Garssen, J., Keshavarzian, A., & Kraneveld, A. D. (2017) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2017.05.042 · Cited by 203 · see citing works
“…by enhancing intestinal epithelial integrity, protecting from barrier disruption, stimulating a healthy homeostasis of the mucosal immune system and suppressing pathogenic bacterial growth (Ait-Belgnaoui et al., 2012; Corridoni et al., 2012; Patel et al., 2012; Sartor, 2005; Zareie et al., 2006).”
BackgroundCrosstalk between the microbiota-gut-brain axis and depression
Du, Y., Gao, X.-R., Peng, L., & Ge, J.-F. (2020) · Heliyon · doi:10.1016/j.heliyon.2020.e04097 · Cited by 191 · see citing works
Jašarević, E., Howard, C. D., Morrison, K., Misic, A., Weinkopff, T., Scott, P., Hunter, C., Beiting, D., & Bale, T. L. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0182-5 · Cited by 189 · see citing works
Kato-Kataoka, A., Nishida, K., Takada, M., Suda, K., Kawai, M., Shimizu, K., Kushiro, A., Hoshi, R., Watanabe, O., Igarashi, T., et al. (2016) · Beneficial Microbes · doi:10.3920/bm2015.0100 · Cited by 166 · see citing works
Javurek, A. B., Spollen, W. G., Johnson, S. A., Bivens, N. J., Bromert, K. H., Givan, S. A., & Rosenfeld, C. S. (2016) · Gut Microbes · doi:10.1080/19490976.2016.1234657 · Cited by 160 · see citing works
Wei, C.-L., Wang, S., Yen, J.-T., Cheng, Y.-F., Liao, C.-L., Hsu, C.-C., Wu, C.-C., & Tsai, Y.-C. (2019) · Brain Research · doi:10.1016/j.brainres.2019.01.025 · Cited by 150 · see citing works
Fecal Microbiota Transplantation and Its Usage in Neuropsychiatric Disorders
Evrensel, A., & Ceylan, M. E. (2016) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2016.14.3.231 · Cited by 150 · see citing works
Psychobiotics: A new approach for treating mental illness?
Misra, S., & Mohanty, D. (2019) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2017.1399860 · Cited by 142 · see citing works
The role of microbes and autoimmunity in the pathogenesis of neuropsychiatric illness
Hornig, M. (2013) · Current Opinion in Rheumatology · doi:10.1097/bor.0b013e32836208de · Cited by 138 · see citing works
Reis, D. J., Ilardi, S. S., & Punt, S. E. W. (2018) · PLOS ONE · doi:10.1371/journal.pone.0199041 · Cited by 123 · see citing works
Stress matters: randomized controlled trial on the effect of probiotics on neurocognition
Papalini, S., Michels, F., Kohn, N., Wegman, J., van Hemert, S., Roelofs, K., Arias-Vasquez, A., & Aarts, E. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.100141 · Cited by 123 · see citing works
Liu, J., Buisman-Pijlman, F., & Hutchinson, M. R. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00309 · Cited by 119 · see citing works
Gut microbiota of mice putatively modifies amino acid metabolism in the host brain
Kawase, T., Nagasawa, M., Ikeda, H., Yasuo, S., Koga, Y., & Furuse, M. (2017) · British Journal of Nutrition · doi:10.1017/s0007114517000678 · Cited by 119 · see citing works
Microbiota, immunoregulatory old friends and psychiatric disorders
Rook, G. A. W., Raison, C. L., & Lowry, C. A. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-0897-4_15 · Cited by 117 · see citing works
Bloemendaal, M., Szopinska-Tokov, J., Belzer, C., Boverhoff, D., Papalini, S., Michels, F., van Hemert, S., Arias Vasquez, A., & Aarts, E. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01404-9 · Cited by 118 · see citing works
Medina-Rodriguez, E. M., Madorma, D., O’Connor, G., Mason, B. L., Han, D., Deo, S. K., Oppenheimer, M., Nemeroff, C. B., Trivedi, M. H., Daunert, S., et al. (2020) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2020.19090960 · Cited by 110 · see citing works
Depressed gut? The microbiota-diet-inflammation trialogue in depression
Koopman, M., & El Aidy, S. (2017) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000350 · Cited by 114 · see citing works
Vodička, M., Ergang, P., Hrnčíř, T., Mikulecká, A., Kvapilová, P., Vagnerová, K., Šestáková, B., Fajstová, A., Hermanová, P., Hudcovic, T., et al. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.07.007 · Cited by 112 · see citing works
Gut microbiota and central nervous system development
Principi, N., & Esposito, S. (2016) · Journal of Infection · doi:10.1016/j.jinf.2016.09.010 · Cited by 92 · see citing works
Gut microbiota regulates key modulators of social behavior
Parashar, A., & Udayabanu, M. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.11.002 · Cited by 88 · see citing works
Bested, A. C., Logan, A. C., & Selhub, E. M. (2013) · Gut Pathogens · doi:10.1186/1757-4749-5-4 · Cited by 84 · see citing works
Visceral Inflammation and Immune Activation Stress the Brain
Holzer, P., Farzi, A., Hassan, A. M., Zenz, G., Jačan, A., & Reichmann, F. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01613 · Cited by 84 · see citing works
Efficacy of probiotics on anxiety-A meta-analysis of randomized controlled trials
Liu, B., He, Y., Wang, M., Liu, J., Ju, Y., Zhang, Y., Liu, T., Li, L., & Li, Q. (2018) · Depression and Anxiety · doi:10.1002/da.22811 · Cited by 81 · see citing works
Andersson, H., Tullberg, C., Ahrné, S., Hamberg, K., Lazou Ahrén, I., Molin, G., Sonesson, M., & Håkansson, Å. (2016) · International Journal of Microbiology · doi:10.1155/2016/8469018 · Cited by 73 · see citing works
Salami, M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.613120 · Cited by 67 · see citing works
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64 · see citing works
The microbiome and disorders of the central nervous system
Felice, V. D., & O'Mahony, S. M. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.016 · Cited by 60 · see citing works
Markey, L., Hooper, A., Melon, L. C., Baglot, S., Hill, M. N., Maguire, J., & Kumamoto, C. A. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104808 · Cited by 45 · see citing works
Keskitalo, A., Aatsinki, A.-K., Kortesluoma, S., Pelto, J., Korhonen, L., Lahti, L., Lukkarinen, M., Munukka, E., Karlsson, H., & Karlsson, L. (2021) · Stress · doi:10.1080/10253890.2021.1895110 · Cited by 44 · see citing works
The gut microbiota affects corticosterone production in the murine small intestine
Ergang, P., Vagnerová, K., Hermanová, P., Vodička, M., Jágr, M., Šrůtková, D., Dvořáček, V., Hudcovic, T., & Pácha, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084229 · Cited by 37 · see citing works
Wauters, L., Van Oudenhove, L., Accarie, A., Geboers, K., Geysen, H., Toth, J., Luypaerts, A., Verbeke, K., Smokvina, T., Raes, J., et al. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2031695 · Cited by 34 · see citing works
Narrative review on potential role of gut microbiota in certain substance addiction
Qin, C., Hu, J., Wan, Y., Cai, M., Wang, Z., Peng, Z., Liao, Y., Li, D., Yao, P., Liu, L., et al. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110093 · Cited by 32 · see citing works
Chan, D. G., Ventura, K., Villeneuve, A., Du Bois, P., & Holahan, M. R. (2022) · Journal of Parkinson's Disease · doi:10.3233/jpd-223461 · Cited by 24 · see citing works
Wang, H.-X., & Wang, Y.-P. (2016) · Chinese Medical Journal · doi:10.4103/0366-6999.190667 · Cited by 546 · see citing works
- Authors
- Ait-Belgnaoui, A., Durand, H., Cartier, C., Chaumaz, G., Eutamene, H., Ferrier, L., Houdeau, E., Fioramonti, J., Bueno, L., & Theodorou, V.
- Affiliations
- Université Toulouse III - Paul Sabatier (FR)
- Lallemand (France) (FR)
- ORCID
- Ferrier, Laurent
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2012-11
- Volume
- 37
- Issue
- 11
- Pages
- 1885-1895
- ISSN
- 0306-4530 (ISSN-L)
- OpenAlex
- W2091052564
- Cited by
- 612
- References
- 58
- Citations by year
- 2026: 19 · 2025: 36 · 2024: 51 · 2023: 48 · 2022: 70 · 2021: 63 · 2020: 53 · 2019: 48 · 2018: 59 · 2017: 39 · 2016: 43 · 2015: 37 · 2014: 23 · 2013: 15 · 2012: 5
- FWCI
- 39.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Institut Rosell-Lallemand
- INRA
- Midi-Pyrenees Region
- “Groupe Français de Neuro-Gastroentérologie”
- Functional Brain-Gut Research Group
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- probiotics, Lactobacillus farciminis, leaky gut, intestinal permeability, hypothalamic-pituitary-adrenal axis, acute psychological stress, lipopolysaccharide translocation, endotoxemia, neuroinflammation, corticosterone, ACTH, corticotropin-releasing factor, myosin light chain kinase, antibiotic-induced dysbiosis, gut-brain axis, depression
- MeSH terms
- Acute Disease, Adrenocorticotropic Hormone, Animals, Anti-Bacterial Agents, Azepines, Colon, Corticosterone, Corticotropin-Releasing Hormone, Female, Hypothalamo-Hypophyseal System, Inflammation, Lactobacillus, Lipopolysaccharides, Myosin-Light-Chain Kinase, Naphthalenes, Permeability, Pituitary-Adrenal System, Restraint, Physical, Stress, Psychological, Cytokines, Rats, Wistar, Probiotics, Rats
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