UNCORRECTED PROOF
Neuroscience Letters xxx (xxxx) xxx-xxx
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Neuroscience Letters
journal homepage: www.elsevier.com
Heat-killed Enterococcus fecalis (EC-12) supplement alters the expression of
neurotransmitter receptor genes in the prefrontal cortex and alleviates anxiety-like
behavior in mice
Jun Kambe
a
, Sovijit Watcharin
a
, Yuko Makioka-Itaya
b
, Ryo Inoue
c
, Gen Watanabe
a
, Hirohito Yamaguchi
d
,
Kentaro Nagaoka
a,
a
Laboratory of Veterinary Physiology, Tokyo University of Agriculture and Technology, Tokyo, Japan
b
Functional Foods, Combi Corporation, Saitama, Japan
c
Laboratory of Animal Science, Kyoto Prefectural University, Kyoto, Japan
d
Cancer Research Center, Qatar Biomedical Research Institute, Hamad Bin Khalifa University, Qatar
ARTICLE INFO
Keywords:
Gut microbiota
Probiotics
EC-12
Anxiety
Depression
ABSTRACT
Gut microbiota plays a crucial role in the maintenance of mental health and inUuences mental disorders such
as depression and anxiety. Several studies have reported the beneTcial affects of probiotics in mental health.
Heat-killed Enterococcus faecalis strain EC-12 (EC-12), a lactic acid bacterium induces activation of the immune
system. However, little is known about the effect of EC-12 on mental health. In the present study, the anti-anxiety
effect of EC-12 was elucidated in vivo. Male mice fed on diet supplemented with EC-12 showed decreased anx-
iety-like behavior in open-Teld and elevated plus-maze tests. In addition, EC-12 supplementation exhibited an
anti-depressive trend in mice subjected to forced swim test. The expression of neurotransmitter receptor genes:
Adrb3 and Avpr1a were significantly enhanced in EC-12 supplemented mice compared to that of the control
mice. In mice, analyses of gut microbiota composition by next generation sequencing revealed significant in-
crease in Butyricicoccus and Enterococcus with EC-12 supplementation. Significant difference was not detected
in the expression of neurotransmitter receptor genes in the prefrontal cortex with the administration of sodium
butyrate compared to that of the control group. The mechanism associated with EC-12 mediated reduced anx-
iety-like behavior and altered gene expression in the brain needs to be further elucidated. Taken together, the
present study is the Trst to report the possibility of exploiting the anti-anxiety effect of heat-killed EC-12 as a
novel probiotic to promote mental health.
1. Introduction
Mental health is a growing concern worldwide as people affected
with depression and anxiety is on the rise globally. A survey con-
ducted by World Health Organization reported 10 % of respondents
with symptoms of depression and anxiety [1]. The cause of depres-
sion and anxiety has been hypothesized to be associated with stress,
hormonal dysfunction, and inUammation [2 4]. Recent research fo-
cusing on the role of gut microbiota on human health has received
a great deal of attention. Evidences gathered from improved molec-
ular tools, metagenomic studies, and animal models have indicated
a strong link between the gut microbiota composition and mental
health (gut microbiota-brain axis) [5,6]. Lower richness and diversity of
gut microbiota was seen in patients with depression compared to that
of healthy individuals matched for gender, age, and ethnicity [7]. Stud-
ies in germ-free (GF) mice have reported reduced depression- and anx-
iety-like behaviors [8,9]. Transplantation of fecal microbiota from de-
pressed patients to microbiota-depleted rodents induced behavioral and
physiological features of depression- and anxiety-like behaviors in the
recipient animals [7,9].
Probiotics are bacteria that are intended to confer health beneTts
when consumed. Several human and animal studies have proved the
ability of lactic acid bacteria such as Lactobacillus and Bi>dobacterium
in alleviating the symptoms of depression and anxiety. In stress in-
duced anxious animal models, administration of L. rhamnosus and L.
Corresponding author.
Email address: nagaokak@cc.tuat.ac.jp (K. Nagaoka)
https://doi.org/10.1016/j.neulet.2020.134753
Received 7 November 2019; Received in revised form 28 December 2019; Accepted 9 January 2020
Available online xxx
0304-3940/ © 2020.
Research article