Indole, a Signaling Molecule Produced by the Gut Microbiota, Negatively Impacts Emotional Behaviors in Rats

Abel, 1995, Behavioral effects of isatin on open field activity and immobility in the forced swim test in rats, Physiol. Behav., 57, 611, 10.1016/0031-9384(94)00365-C

Altieri, 2011, Urinary p-cresol is elevated in small children with severe autism spectrum disorder, Biomarkers, 16, 252, 10.3109/1354750X.2010.548010

Armario, 2012, What can we know from pituitary-adrenal hormones about the nature and consequences of exposure to emotional stressors?, Cell. Mol. Neurobiol., 32, 749, 10.1007/s10571-012-9814-6

Baba, 2006, Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection, Mol. Syst. Biol., 2, 2006, 10.1038/msb4100050

Bansal, 2010, The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation, Proc. Natl. Acad. Sci. U.S.A., 107, 228, 10.1073/pnas.0906112107

Bhattacharya, 1991, Anxiogenic activity of isatin, a putative biological factor, in rodents, J. Psychopharmacol., 5, 202, 10.1177/026988119100500304

Bravo, 2011, Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve, Proc. Natl. Acad. Sci. U.S.A., 108, 16050, 10.1073/pnas.1102999108

Carpenedo, 1998, Oxindole, a sedative tryptophan metabolite, accumulates in blood and brain of rats with acute hepatic failure, J. Neurochem., 70, 1998, 10.1046/j.1471-4159.1998.70051998.x

Cecchi, 2002, Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress, Neuroscience, 112, 13, 10.1016/S0306-4522(02)00062-3

Chermat, 1986, Adaptation of the tail suspension test to the rat, J. Pharmacol., 17, 348

Chimerel, 2014, Bacterial metabolite indole modulates incretin secretion from intestinal enteroendocrine L cells, Cell Rep., 9, 1202, 10.1016/j.celrep.2014.10.032

Clarke, 2013, The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner, Mol. Psychiatry, 18, 666, 10.1038/mp.2012.77

Covasa, 2005, Reduced CCK-induced Fos expression in the hindbrain, nodose ganglia, and enteric neurons of rats lacking CCK-1 receptors, Brain Res., 1051, 155, 10.1016/j.brainres.2005.06.003

Crawley, 1985, Exploratory behavior models of anxiety in mice, Neurosci. Biobehav. Rev., 9, 37, 10.1016/0149-7634(85)90030-2

Crumeyrolle-Arias, 2014, Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats, Psychoneuroendocrinology, 42, 207, 10.1016/j.psyneuen.2014.01.014

Crumeyrolle-Arias, 2003, In situ imaging of specific binding of [3H]isatin in rat brain, J. Neurochem., 84, 618, 10.1046/j.1471-4159.2003.01564.x

Cryan, 2012, Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour, Nat. Rev. Neurosci., 13, 701, 10.1038/nrn3346

Deguchi, 2003, Pharmacokinetics and tissue distribution of uraemic indoxyl sulphate in rats, Biopharm. Drug Dispos., 24, 345, 10.1002/bdd.370

De Palma, 2017, Transplantation of fecal microbiota from patients with irritable bowel syndrome alters gut function and behavior in recipient mice, Sci. Transl. Med., 9, eaaf6397, 10.1126/scitranslmed.aaf6397

De Vadder, 2014, Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits, Cell, 156, 84, 10.1016/j.cell.2013.12.016

Ennaceur, 1988, A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data, Behav. Brain Res., 31, 47, 10.1016/0166-4328(88)90157-X

Ennaceur, 2005, Detailed analysis of the behavior of Lister and Wistar rats in anxiety, object recognition and object location tasks, Behav. Brain Res., 159, 247, 10.1016/j.bbr.2004.11.006

File, 1978, Can social interaction be used to measure anxiety?, Br. J. Pharmacol., 62, 19, 10.1111/j.1476-5381.1978.tb07001.x

Hamaue, 2000, Urinary isatin concentrations in patients with Parkinson's disease determined by a newly developed HPLC-UV method, Res. Commun. Mol. Pathol. Pharmacol., 108, 63

Handley, 1984, Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of 'fear'-motivated behaviour, Naunyn Schmiedebergs. Arch. Pharmacol., 327, 1, 10.1007/BF00504983

Hsiao, 2013, Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders, Cell, 155, 1451, 10.1016/j.cell.2013.11.024

Humblot, 2007, β-Glucuronidase in human intestinal microbiota is necessary for the colonic genotoxicity of the food-borne carcinogen 2-amino-3-methylimidazo[4,5-f]quinoline in rats, Carcinogenesis, 28, 2419, 10.1093/carcin/bgm170

Igosheva, 2004, Effect of acute stress and gender on isatin in rat tissues and serum, Physiol. Behav., 80, 665, 10.1016/j.physbeh.2003.11.005

Jiang, 2015, Altered fecal microbiota composition in patients with major depressive disorder, Brain Behav. Immun., 48, 186, 10.1016/j.bbi.2015.03.016

Katoh, 2002, MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform, Nucleic Acids Res., 30, 3059, 10.1093/nar/gkf436

Keck, 2003, Reduction of hypothalamic vasopressinergic hyperdrive contributes to clinically relevant behavioral and neuroendocrine effects of chronic paroxetine treatment in a psychopathological rat model, Neuropsychopharmacology, 28, 235, 10.1038/sj.npp.1300040

Kelly, 2016, Transferring the blues: depression-associated gut microbiota induces neurobehavioural changes in the rat, J. Psychiatr. Res., 82, 109, 10.1016/j.jpsychires.2016.07.019

Krstulovic, 1979, Rapid analysis of tryptophan metabolites using reversed-phase high-performance liquid chromatography with fluorometric detection, J. Chromatogr., 163, 72, 10.1016/S0378-4347(00)81170-6

Lee, 2010, Indole as an intercellular signal in microbial communities, FEMS Microbiol. Rev., 34, 426, 10.1111/j.1574-6976.2009.00204.x

Lee, 2015, Roles of indole as an interspecies and interkingdom signaling molecule, Trends Microbiol., 23, 707, 10.1016/j.tim.2015.08.001

Lee, 2008, Repeated stimulation of CRF receptors in the BNST of rats selectively induces social but not panic-like anxiety, Neuropsychopharmacology, 33, 2586, 10.1038/sj.npp.1301674

Li, 2014, An integrated catalog of reference genes in the human gut microbiome, Nat. Biotechnol., 32, 834, 10.1038/nbt.2942

Lozupone, 2012, Diversity, stability and resilience of the human gut microbiota, Nature, 489, 220, 10.1038/nature11550

Manabe, 1997, Determination of isatin in urine and plasma by high-performance liquid chromatography, J. Chromatogr. B. Biomed. Sci. Appl., 691, 197, 10.1016/S0378-4347(96)00409-4

Marcobal, 2013, A metabolomic view of how the human gut microbiota impacts the host metabolome using humanized and gnotobiotic mice, ISME J., 7, 1933, 10.1038/ismej.2013.89

Mingam, 2008, Uncoupling of interleukin-6 from its signalling pathway by dietary n-3-polyunsaturated fatty acid deprivation alters sickness behaviour in mice, Eur. J. Neurosci., 28, 1877, 10.1111/j.1460-9568.2008.06470.x

Moroni, 1998, Oxindole in pathogenesis of hepatic encephalopathy, Lancet, 351, 1861, 10.1016/S0140-6736(05)78807-3

Naseribafrouei, 2014, Correlation between the human fecal microbiota and depression, Neurogastroenterol. Motil., 26, 1155, 10.1111/nmo.12378

Nicholson, 2005, Gut microorganisms, mammalian metabolism and personalized health care, Nat. Rev. Microbiol., 3, 431, 10.1038/nrmicro1152

Nishino, 2013, Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods, Neurogastroenterol. Motil., 25, 521, 10.1111/nmo.12110

O'Mahony, 2015, Serotonin, tryptophan metabolism and the brain-gut-microbiome axis, Behav. Brain Res., 277, 32, 10.1016/j.bbr.2014.07.027

Paxinos, 2005, The Rat Brain in Stereotaxic Coordinates, 5th Edn.

Pinto-Sanchez, 2017, Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome, Gastroenterology, 153, 448, 10.1053/j.gastro.2017.05.003

Ramos, 1997, A multiple-test study of anxiety-related behaviours in six inbred rat strains, Behav. Brain Res., 85, 57, 10.1016/S0166-4328(96)00164-7

Rothhammer, 2016, Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor, Nat. Med., 22, 586, 10.1038/nm.4106

Sasaki-Imamura, 2011, Molecular basis of indole production catalyzed by tryptophanase in the genus Prevotella, FEMS Microbiol. Lett., 322, 51, 10.1111/j.1574-6968.2011.02329.x

Satyan, 1995, Isatin, a putative anxiogenic endocoid, induces memory dysfunction in rats, Indian, J. Exp. Biol., 33, 576

Schroeder, 2016, Signals from the gut microbiota to distant organs in physiology and disease, Nat. Med., 22, 1079, 10.1038/nm.4185

Sharon, 2014, Specialized metabolites from the microbiome in health and disease, Cell Metab., 20, 19, 10.1016/j.cmet.2014.10.016

Slotten, 2006, Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects, Brain Res., 1097, 123, 10.1016/j.brainres.2006.04.066

Stappenbeck, 2002, Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells, Proc. Natl. Acad. Sci. U.S.A., 99, 15451, 10.1073/pnas.202604299

Stilling, 2016, The neuropharmacology of butyrate: the bread and butter of the microbiota-gut-brain axis?, Neurochem. Int., 99, 110, 10.1016/j.neuint.2016.06.011

Sudo, 2004, Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice, J. Physiol., 558, 263, 10.1113/jphysiol.2004.063388

Sundquist, 2005, Fast Fos: rapid protocols for single- and double-labeling c-Fos immunohistochemistry in fresh frozen brain sections, J. Neurosci. Methods, 141, 9, 10.1016/j.jneumeth.2004.05.007

Thompson, 1994, CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res., 22, 4673, 10.1093/nar/22.22.4673

Valdés-Cruz, 2002, Chronic stimulation of the cat vagus nerve: effect on sleep and behavior, Prog. Neuropsychopharmacol. Biol. Psychiatry, 26, 113, 10.1016/S0278-5846(01)00228-7

Wigger, 1999, Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats, Physiol. Behav., 66, 293, 10.1016/S0031-9384(98)00300-X

Wikoff, 2009, Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites, Proc. Natl. Acad. Sci. U.S.A., 106, 3698, 10.1073/pnas.0812874106

Yang, 2004, Peripheral secretin-induced Fos expression in the rat brain is largely vagal dependent, Neuroscience, 128, 131, 10.1016/j.neuroscience.2004.06.027

Yap, 2010, Urinary metabolic phenotyping differentiates children with autism from their unaffected siblings and age-matched controls, J. Proteome Res., 9, 2996, 10.1021/pr901188e

Yoshida, 2009, Identification and molecular characterization of tryptophanase encoded by tnaA, Porphyromonas gingivalis. Microbiology, 155, 968, 10.1099/mic.0.024174-0

Zheng, 2016, Gut microbiome remodeling induces depressive-like behaviors through a pathway mediated by the host's metabolism, Mol. Psychiatry., 21, 786, 10.1038/mp.2016.44