Pubertal probiotic blocks LPS-induced anxiety and the associated neurochemical and microbial outcomes, in a sex dependent manner

Murray, E. Selkirk; Smith, Kevin B.; Stoby, Karlene S.; Thomas, Bronwen J.; Swenson, Michael J.; Arber, L.; Frenette, Emilie; Ismail, Nafissa

doi:10.1016/j.psyneuen.2019.104481

Cited by 33 publications

(34 citation statements)

References 52 publications

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“…Since Lactobacillus has been shown to decrease in response to a psychological challenge, it has been used as a probiotic in humans and experimental animals to improve behavioral abnormalities 27 . For example, Lactobacillus johnsonii has been shown to attenuate stress-induced and intraperitoneal injection of LPS-induced anxiety-like behavior in male mice 28 ; Lactobacillus rhamnosus reduced stress-induced anxiety-and depression-related behavior in male mice 29 ; Supplementation of Lactobacillus reuteri prevented longstanding LPS-induced changes in anxiety-like behavior and stress-induced brain activation in male mice 30 . Together with these reports, our results demonstrated that male, but not female mice with chronic nasal inflammation are likely to suffer from chronic stress.…”

Section: Discussionmentioning

confidence: 99%

Sex-dependent differences in the gut microbiota following chronic nasal inflammation in adult mice

Mishima

Osaki

Shimada

et al. 2021

Sci Rep

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A growing body of evidence suggests a relationship between olfactory dysfunction and the pathogenesis of mental disorders. Our previous studies indicated that chronic nasal inflammation caused loss of olfactory sensory neurons and gross atrophy of the olfactory bulb, which may lead to olfactory dysfunction. Simultaneously, increasing numbers of reports have elucidated the importance of gut microbiota to maintain brain function and that dysbiosis may be associated with neuropsychiatric disorders. Here we examined whether chronic nasal inflammation perturbed gut microbiota and whether there were sex differences in this pattern. Eight-week-old C57BL/6 mice repeatedly received bilateral nasal administration of lipopolysaccharide (LPS) 3 times/week to cause chronic nasal inflammation or saline as a control. At 9 weeks, cecal feces were used for 16S metagenomic analysis and whole blood and fresh tissue of spleen were used for ELISA analyses. Microbiome analysis demonstrated a remarkable change of the gut microbiota in male mice with chronic nasal inflammation which was different from that in female mice. In both mice, systemic inflammation did not occur. This has shown for the first time that chronic nasal inflammation correlates with sex-dependent changes in the gut microbiota. The detailed mechanism and potential alteration to brain functions await further studies.

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Section: Discussionmentioning

confidence: 99%

Sex-dependent differences in the gut microbiota following chronic nasal inflammation in adult mice

Mishima

Osaki

Shimada

et al. 2021

Sci Rep

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“…As we expected, this study found that THPH administration altered gut microbiota diversity in cognitive impairment mice, including increasing the abundance of Actinobacterota , which produced metabolites with anti-AchE activity [ 62 ]. THPH treatment also increased the abundance of probiotics, such as Lactobacillus reuteri and Prevotellaceae UCG-001 , which had the effects of regulating neural behavior and improving cognitive function, and produced metabolites that participated in the hosts’ lipid metabolism to maintain the brain function [ 63 , 64 , 65 , 66 ]. In addition, THPH reduced the severity of gut microbiota dysbiosis by altering the structure of the microbial community via the decreased abundance of pathobionts, including Desulfovibrionales , Desulfovibrionaceae , and Anaerotruncus , which related to cognition and neurodegenerative diseases.…”

Section: Discussionmentioning

confidence: 99%

Tilapia Head Protein Hydrolysate Attenuates Scopolamine-Induced Cognitive Impairment through the Gut-Brain Axis in Mice

Zhu

et al. 2021

Foods

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The destruction of the homeostasis in the gut-brain axis can lead to cognitive impairment and memory decline. Dietary intervention with bioactive peptides from aquatic products is an innovative strategy to prevent cognitive deficits. The present study aimed to determine the neuroprotective effect of tilapia head protein hydrolysate (THPH) on scopolamine-induced cognitive impairment in mice, and to further explore its mechanism through the microbiota–gut-brain axis. The results showed that THPH administration significantly improved the cognitive behavior of mice, and normalized the cholinergic system and oxidative stress system of the mice brain. The histopathological observation showed that THPH administration significantly reduced the pathological damage of hippocampal neurons, increased the number of mature neurons marked by NeuN and delayed the activation of astrocytes in the hippocampus of mice. In addition, THPH administration maintained the stability of cholinergic system, alleviated oxidative stress and further improved the cognitive impairment by reshaping the gut microbiota structure of scopolamine-induced mice and alleviating the disorder of lipid metabolism and amino acid metabolism in serum. In conclusion, our research shows that THPH supplementation is a nutritional strategy to alleviate cognitive impairment through the gut-brain axis.

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“…Sex-specific differences in the gut-brain axis have been reported, and these differences are thought to contribute to the discrepancies in neuroinflammation and the incidence of psychiatric disorders between sexes (reviewed in Holingue et al, 2020;Jaggar et al, 2020;Jasarevic et al, 2016;Kim et al, 2020). Consistently, the effects of nutritional interventions or gut microbiome manipulations on the immune system, brain functions, and psychological behaviors were also sex-specifically different in animal studies (Christoforidou et al, 2019;Darch et al, 2021;Miao et al, 2016;Murray et al, 2020;Surzenko et al, 2020;Zhang et al, 2018). The sex disparity in immune development, immune response, and probiotics/gut microbiome response could be linked to differences in sex hormones.…”

Section: Limitations Of This Studymentioning

confidence: 98%

“…Consistently, treatments with probiotics, a combination of beneficial live bacteria and/or yeasts, have been reported to improve intestinal and immune homeostasis and exert ameliorative effects on aspects of neuropsychiatric conditions in patients and animal studies (Azad et al., 2018; Bravo et al., 2011; Cowan et al., 2016; Desbonnet et al., 2010; Dickerson et al., 2018; Kunze et al., 2009; Ligezka et al., 2020; Mehrabadi & Sadr, 2020; Naveed et al., 2021; Nishida et al., 2019; Pandey et al., 2015; Park et al., 2020; Rajanala et al., 2020; Rao et al., 2009; Rezaei Asl et al., 2019; Rezaeiasl et al., 2019; Stavropoulou & Bezirtzoglou, 2020). Probiotics are also known to decrease anxiety in several preclinical mouse models including BALB/c mice characterized by elevated anxiety (Barros‐Santos et al., 2020; Han & Kim, 2019; Jang et al., 2019; Murray et al., 2019, 2020; Savignac et al., 2014, 2015; Surzenko et al., 2020). However, since no manipulations of the gut microbiome were attempted in these studies, it remains unclear as to what role the gut microbiome could play in modulating the effects of probiotics on psychological or psychiatric behaviors with respect to any electrophysiological changes in neurons.…”

Section: Introductionmentioning

confidence: 99%

Homeostatic regulation of neuronal excitability by probiotics in male germ‐free mice

Kim

Lee

et al. 2021

J of Neuroscience Research

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Emerging evidence indicates that probiotics can influence the gut–brain axis to ameliorate somatic and behavioral symptoms associated with brain disorders. However, whether probiotics have effects on the electrophysiological activities of individual neurons in the brain has not been evaluated at a single‐neuron resolution, and whether the neuronal effects of probiotics depend on the gut microbiome status have yet to be tested. Thus, we conducted whole‐cell patch‐clamp recording‐assisted electrophysiological characterizations of the neuronal effects of probiotics in male germ‐free (GF) mice with and without gut microbiome colonization. Two weeks of treatment with probiotics (Lactobacillus rhamnosus and Bifidobacterium animalis) significantly and selectively increased the intrinsic excitability of hippocampal CA1 pyramidal neurons, whereas reconstituting gut microbiota in GF mice reversed the effects of the probiotics leading to a decreased intrinsic excitability in hippocampal neurons. This bidirectional modulation of neuronal excitability by probiotics was observed in hippocampal neurons with corresponding basal membrane property and action potential waveform changes. However, unlike the hippocampus, the amygdala excitatory neurons did not show any electrophysiological changes to the probiotic treatment in either GF or conventionalized GF mice. Our findings demonstrate for the first time how probiotic treatment can have a significant influence on the electrophysiological properties of neurons, bidirectionally modulating their intrinsic excitability in a gut microbiota and brain area‐specific manner.

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Pubertal probiotic blocks LPS-induced anxiety and the associated neurochemical and microbial outcomes, in a sex dependent manner

Cited by 33 publications

References 52 publications

Sex-dependent differences in the gut microbiota following chronic nasal inflammation in adult mice

Sex-dependent differences in the gut microbiota following chronic nasal inflammation in adult mice

Tilapia Head Protein Hydrolysate Attenuates Scopolamine-Induced Cognitive Impairment through the Gut-Brain Axis in Mice

Homeostatic regulation of neuronal excitability by probiotics in male germ‐free mice

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