Patient-derived Enterococcus mundtii and its capsular polysaccharides cause depression through the downregulation of NF-κB-involved serotonin and BDNF expression

Joo, Min Kyung; Ma, Xiaoyang; Yoo, Jong-Wook; Shin, Yoon-Jung; Kim, Hyo-Jong; Kim, Dong-Hyun

doi:10.1016/j.micinf.2023.105116

Cited by 15 publications

(14 citation statements)

References 45 publications

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“… 10 Pathogenic Enterococcus species, such as EM, Enterococcus durans and Enterococcus gallinarum increase pro-inflammatory cytokine expression and decrease brain-derived neurotrophic factor (BDNF) protein levels in the hippocampus of mice with depression. 43 In this study involving patients with UC, we also found that EM, belonging to Enterococcaceae , reduced the levels of anti-depressive NPY in the colon, plasma, and hippocampus, causing anxiety and depression-like behavior. Thus, the pathogenicity of enterococci may be associated with a direct and/or indirect effect of EM on, both, the colon and brain, resulting in psychiatric disorders, such as anxiety and depression.…”

Section: Discussionmentioning

confidence: 61%

“…Previously, we demonstrated that the oral administration of gut bacteria EC, KO, and EM (NK1516) isolated from the feces of patients with IBD causes UC-like inflammation and depression-like behavior in mice. 42 , 43 In this study, we specifically explored the relationship between gut bacteria and NPY expression and production in the colon. We first verified that EC, KO, and EM induced colitis- and anxiety/depression-like behavior ( Figure 4a and Supplementary Figure S3).…”

Section: Resultsmentioning

confidence: 99%

“…Previously, we found that capsular polysaccharides (CPs) of EM (NK1516) isolated from patients with IBD play a critical role in inducing anxiety- and depression-like behavior in mice. 43 To investigate whether the CP of EM (NK1516-CP) was associated with NPY levels in mice, we orally administered NK1516-CP and observed anxiety- and depression-like behavior, similar to those induced by EM ( Figure 6a and Supplementary Figure S5A and S5B). We also found that NK1516-CP significantly decreased NPY levels in the colon, plasma, and brain of mice ( Figure 6b–d ).…”

Section: Resultsmentioning

confidence: 99%

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Regulation of colonic neuropeptide Y expression by the gut microbiome in patients with ulcerative colitis and its association with anxiety- and depression-like behavior in mice

Joo,

Lee,

Woo

et al. 2024

Gut Microbes

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Patients with inflammatory bowel disease (IBD), including ulcerative colitis (UC), show an increased incidence of anxiety and depression; however, the association between UC-associated psychiatric disorders and the gut microbiota is unclear. This study aimed to examine whether gut microbiota from patients with UC can alter colonic gene expression, leading to anxiety- and depression-like behavior in mice receiving fecal microbiota transplantation (FMT). RNA sequencing transcriptome analyses revealed a difference in colonic gene expression between mice receiving FMT from patients with UC (UC-FMT mice) and those receiving FMT from healthy controls (HC-FMT mice). Gene ontology analysis revealed the downregulation of neuropeptide signaling pathways, including neuropeptide Y (NPY) expression, in the colons of UC-FMT mice. The protein levels of NPY also decreased in the colon and plasma of UC-FMT mice compared to those in HC-FMT mice. The oral administration of Enterococcus mundtii (EM), a bacterium isolated from the feces of patients with UC, reduced NPY expression in the colons of mice and induced intestinal inflammation, anxiety, and depression-like behavior. Reduced NPY protein levels were also observed in the plasma and hippocampus of EM-treated mice. Intraperitoneal administration of NPY significantly alleviated anxiety- and depressive-like behaviors induced by EM in mice. Capsular polysaccharide in EM was associated with EM-induced NPY downregulation in the colon. Analysis of Gene Expression Omnibus datasets showed markedly reduced NPY expression in the inflamed colons of patients with UC compared with that in the colons of healthy controls. In summary, EM-induced reduction in the colonic expression of NPY may be associated with a decrease in hippocampal NPY and anxiety- and depression-like behavior in mice.

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Section: Discussionmentioning

confidence: 61%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Regulation of colonic neuropeptide Y expression by the gut microbiome in patients with ulcerative colitis and its association with anxiety- and depression-like behavior in mice

Joo,

Lee,

Woo

et al. 2024

Gut Microbes

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“…Herein, the abundance of Phascolarctobacterium in the HSP40-0, HSP60-0, and HSP80-0 groups (2.98, 12.45, and 5.90%, respectively) significantly increased compared with that in the BLK group (0.78%). According to the previous research, typically, more Enterococcus in feces from depressed patients was observed compared with that in a healthy group . The relative abundance of Enterococcus in HSP groups was markedly lower than that in the BLK group.…”

Section: Resultsmentioning

confidence: 80%

“…According to the previous research, typically, more Enterococcus in feces from depressed patients was observed compared with that in a healthy group. 31 The relative abundance of Enterococcus in HSP groups was markedly lower than that in the BLK group. Furthermore, as a core member of the gut microbiota, Parabacteroides could regulate the anti-inflammatory response and secretion of SCFAs.…”

Section: Effects Of Hsps On Microbial Compositionmentioning

confidence: 90%

The Regulatory Effect of Huangshui Polysaccharides on Intestinal Microbiota and Metabolites during In Vitro Fermentation

Li,

Su,

et al. 2024

J. Agric. Food Chem.

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Huangshui polysaccharides (HSPs) have attracted extensive attention recently for their biological activity and physicochemical property. This research investigated the extraction, structural characterization, and prebiotic activity of three different HSPs (HSP40-0, HSP60-0, and HSP80-0) in vitro to reveal the scientific support for the high-value utilization of Huangshui. HSPs were heteropolysaccharide with diverse structures and surface morphologies. Comprehensive analysis was conducted through 16S rRNA gene sequencing and metabolite profiling techniques, and results showed that HSPs had different potentials to regulate the gut microbiota due to their different structures; for instance, both HSP40-0 and HSP80-0 could notably increase the relative abundance of Bacteroidota, whereas HSP60-0 could increase the relative abundance of Phascolarctobacterium. In addition, HSPs upregulated beneficial differential metabolites, especially short-chain fatty acids (SCFAs). Fermentation products containing these metabolites exhibited anti-inflammatory effects on LPS-treated Caco-2 cells. This study will provide reference for exploring the relationship between the natural polysaccharide structure and the prebiotic activity and widen the application of Huangshui.

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Effect of gut microbiome on serotonin metabolism: a personalized treatment approach

Potter,

Gayle,

Deb

2023

Naunyn-Schmiedeberg's Arch Pharmacol

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Patient-derived Enterococcus mundtii and its capsular polysaccharides cause depression through the downregulation of NF-κB-involved serotonin and BDNF expression

Cited by 15 publications

References 45 publications

Regulation of colonic neuropeptide Y expression by the gut microbiome in patients with ulcerative colitis and its association with anxiety- and depression-like behavior in mice

Regulation of colonic neuropeptide Y expression by the gut microbiome in patients with ulcerative colitis and its association with anxiety- and depression-like behavior in mice

The Regulatory Effect of Huangshui Polysaccharides on Intestinal Microbiota and Metabolites during In Vitro Fermentation

Effect of gut microbiome on serotonin metabolism: a personalized treatment approach

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