Mom’s diet matters: Maternal prebiotic intake in mice reduces anxiety and alters brain gene expression and the fecal microbiome in offspring

Hebert, Jenna C.; Radford-Smith, Daniel E.; Probert, Fay; Ilott, Nicholas E.; Chan, Ka Wai; Anthony, Daniel C.; Burnet, Philip W. J.

doi:10.1016/j.bbi.2020.09.034

Cited by 21 publications

(16 citation statements)

References 74 publications

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“…In this study, expression of the GLUN2A and GLUN2B NMDAR subunits was reduced in the PFC of juvenile probiotic offspring. We previously found that maternal prebiotic supplementation reduced these subunits in the juvenile offspring hippocampus ( 27 ), and others have shown that prebiotic supplementation reduced GLUN2B protein in the frontal cortex ( 41 ) of adult mice. Consistent with our present data in juvenile mice, these reported changes in gene expression were associated with reduced anxiety-like ( 41 ) behavior.…”

Section: Discussionmentioning

confidence: 98%

“…The anxiolytic and antidepressant effects of perinatal probiotic exposure in this study are concordant with reports describing similar behavioral responses in rodent offspring: Lactobacillus helveticus NS8 intake in normal-weight dams from embryonic day (E) 13 to E22 during gestation has been shown to reduce offspring anxiety ( 40 ), and maternal perinatal prebiotic intake (which encourages the growth of endogenous Bifidobacterium spp. ) reduced passive stress coping in the FST in adulthood ( 27 ). Reduced social behavior observed in the adult offspring of obese dams is associated with reduced Bifidobacterium spp.…”

Section: Discussionmentioning

confidence: 99%

“…In unchallenged, wild-type mice, maternal perinatal prebiotic intake reduces offspring anxiety-like behaviors, alters brain N -methyl- d -aspartate receptor (NMDAR) gene expression, and increases fecal short-chain fatty acid (SCFA) levels ( 27 ). In the offspring of obese dams, microbial reconstitution with Lactobacillus reuteri can normalize brain dopaminergic activity and social behavior ( 23 ), although no insight into downstream changes in microbial, or brain, metabolism was presented.…”

mentioning

confidence: 99%

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Modifying the maternal microbiota alters the gut–brain metabolome and prevents emotional dysfunction in the adult offspring of obese dams

Radford-Smith

Probert

Burnet

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Maternal obesity disturbs brain–gut–microbiota interactions and induces negative affect in the offspring, but its impact on gut and brain metabolism in the offspring (F1) are unknown. Here, we tested whether perinatal intake of a multispecies probiotic could mitigate the abnormal emotional behavior in the juvenile and adult offspring of obese dams. Untargeted NMR-based metabolomic profiling and gene-expression analysis throughout the gut–brain axis were then used to investigate the biology underpinning behavioral changes in the dams and their offspring. Prolonged high-fat diet feeding reduced maternal gut short-chain fatty acid abundance, increased markers of peripheral inflammation, and decreased the abundance of neuroactive metabolites in maternal milk during nursing. Both juvenile (postnatal day [PND] 21) and adult (PND112) offspring of obese dams exhibited increased anxiety-like behavior, which were prevented by perinatal probiotic exposure. Maternal probiotic treatment increased gut butyrate and brain lactate in the juvenile and adult offspring and increased the expression of prefrontal cortex PFKFB3, a marker of glycolytic metabolism in astrocytes. PFKFB3 expression correlated with the increase in gut butyrate in the juvenile and adult offspring. Maternal obesity reduced synaptophysin expression in the adult offspring, while perinatal probiotic exposure increased expression of brain-derived neurotrophic factor. Finally, we showed that the resilience of juvenile and adult offspring to anxiety-like behavior was most prominently associated with increased brain lactate abundance, independent of maternal group. Taken together, we show that maternal probiotic supplementation exerts a long-lasting effect on offspring neuroplasticity and the offspring gut–liver–brain metabolome, increasing resilience to emotional dysfunction induced by maternal obesity.

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Section: Discussionmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Modifying the maternal microbiota alters the gut–brain metabolome and prevents emotional dysfunction in the adult offspring of obese dams

Radford-Smith

Probert

Burnet

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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“…In this section, animal studies on administration of prebiotics that led to improvement in AD associated brain disorders are summarized. Bimuno-GOS intake in pregnant mice affected the offspring's exploratory behavior and brain gene expression as well as reducing anxiety [168]. Additionally, fecal butyrate and propionate levels were increased after Bimuno-GOS supplementation in postnatal mice [168].…”

Section: Animal Modelsmentioning

confidence: 99%

“…Bimuno-GOS intake in pregnant mice affected the offspring's exploratory behavior and brain gene expression as well as reducing anxiety [168]. Additionally, fecal butyrate and propionate levels were increased after Bimuno-GOS supplementation in postnatal mice [168]. In another study, behavioral testing was performed on mice from the least stressful (three-chamber test) to the most stressful (forced swim test) for 5 weeks during a 10-week prebiotic administration period including lead-in and lead-out periods [169].…”

Section: Animal Modelsmentioning

confidence: 99%

The Potential Utility of Prebiotics to Modulate Alzheimer’s Disease: A Review of the Evidence

Kang

Zivkovic

2021

Microorganisms

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The gut microbiome has recently emerged as a critical modulator of brain function, with the so-called gut-brain axis having multiple links with a variety of neurodegenerative and mental health conditions, including Alzheimer’s Disease (AD). Various approaches for modulating the gut microbiome toward compositional and functional states that are consistent with improved cognitive health outcomes have been documented, including probiotics and prebiotics. While probiotics are live microorganisms that directly confer beneficial health effects, prebiotics are oligosaccharide and polysaccharide structures that can beneficially modulate the gut microbiome by enhancing the growth, survival, and/or function of gut microbes that in turn have beneficial effects on the human host. In this review, we discuss evidence showing the potential link between gut microbiome composition and AD onset or development, provide an overview of prebiotic types and their roles in altering gut microbial composition, discuss the effectiveness of prebiotics in regulating gut microbiome composition and microbially derived metabolites, and discuss the current evidence linking prebiotics with health outcomes related to AD in both animal models and human trials. Though there is a paucity of human clinical trials demonstrating the effectiveness of prebiotics in altering gut microbiome-mediated health outcomes in AD, current evidence highlights the potential of various prebiotic approaches for beneficially altering the gut microbiota or gut physiology by promoting the production of butyrate, indoles, and secondary bile acid profiles that further regulate gut immunity and mucosal homeostasis, which are associated with beneficial effects on the central immune system and brain functionality.

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Probiotics ameliorates LPS induced neuroinflammation injury on Aβ 1–42, APP, γ-β secretase and BDNF levels in maternal gut microbiota and fetal neurodevelopment processes

Kar¹,

Hacıoğlu

Kar³

et al. 2022

Metab Brain Dis

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Mom’s diet matters: Maternal prebiotic intake in mice reduces anxiety and alters brain gene expression and the fecal microbiome in offspring

Cited by 21 publications

References 74 publications

Modifying the maternal microbiota alters the gut–brain metabolome and prevents emotional dysfunction in the adult offspring of obese dams

Modifying the maternal microbiota alters the gut–brain metabolome and prevents emotional dysfunction in the adult offspring of obese dams

The Potential Utility of Prebiotics to Modulate Alzheimer’s Disease: A Review of the Evidence

Probiotics ameliorates LPS induced neuroinflammation injury on Aβ 1–42, APP, γ-β secretase and BDNF levels in maternal gut microbiota and fetal neurodevelopment processes

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