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In 60Co‐γ ray‐irradiated mice, we investigated the changes in behavior, neurotransmitters and gut microbiota after different days of.
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Official websites use. Share sensitive information only on official, secure websites. Email: lwh hit. Acanthopanax senticosus AS is a medicinal and food plant with many physiological functions, especially nerve protection. Its extract has many functional components, including polysaccharides, flavonoids, saponins, and amino acids. Our previous study indicated that AS extract protected against nerve damage caused by radiation. The AS extract improved learning and memory ability in mice, and the neurotransmitter levels in the hippocampus and colon started to change from the 7th day, which accompanied changes of the gut microbiota, a decreased abundance of Helicobacter on the 7th day and an increased abundance of Lactobacillus on the 28th day. Keywords: Acanthopanax senticosus extract, gut microbiota, learning and memory impairment, neurotransmitters, radiation. By Figdraw www. With the development of science and technology, radiation widely exists in our life. Space radiation, nuclear pollution as well as radiation pollution, all can induce negative effects on the organism, including the endocrine system, circulatory system, and reproductive system, and especially serious damage to the nervous system. It has the highest control ability in learning and memory, cognitive understanding, judgment, and reasoning. Thus, it's crucial to protect our brains from radiation. However, some antiradiation agents are difficult to popularize due to their high side effects and high price. Therefore, exploring antiradiation drugs with high efficiency and low toxicity is in an urge. Many homologous ingredients of medicine and food, such as polysaccharides, flavonoids, saponins, peptides, alkaloids, and vitamins, have been found to have antiradiation activities. Previous studies have confirmed the ability of AS to improve learning and memory, increase the number of neurons, prevent brain damage, and have good therapeutic effects on central degenerative diseases and cerebrovascular diseases. In addition, many studies have shown that gut microbes and their metabolites are extensively involved in the communication between the brain and the gut in recent years. In this study, we explored the changes in neurotransmitters and gut microbiota in irradiated mice treated with AS extract as a dietary supplement from the perspectives of behavior and neurotransmitters. The recommended dose of commercially available Acanthopanax tablets is 1—1. The control group and model group were administrated with saline. The determination of the main compounds in the extracts of Acanthopanax was carried out with minor modifications according to the method described in the Chinese Pharmacopeia. Acetonitrile A and 0. Standard curves were developed for the quantification of the five main active ingredients in the AS extract, protocatechuic acid, syringin, chlorogenic acid, eleutheroside E, isofraxidin using the above method. The content of flavonoids in AS was determined by aluminum nitrate colorimetry, and rutin was used as the standard. Briefly, 0. The spatial learning and memory performance of mice was tested by the water maze. Briefly, the rectangular water maze contained many blind zones and an exit platform. In the experiment, we recorded the time of the mice reaching the platform at the exit and the time of mice hitting the maze wall. The platform arrival time and the number of times to blind zones were recorded. The sensitivity of the nervous system of mice was tested by the sucrose preference test. Sucrose partiality was defined as the ratio of the volume of sucrose vs. After fixation, the tissues were dehydrated and embedded in paraffin. In the neurotransmitter assay, the hippocampus and colon were homogenized with saline and the supernatant was centrifuged, followed by the commercial kit instructions. For the inflammatory cytokine assay in serum, whole blood was collected and the serum was centrifuged for the assay. The specific operation followed the protocol of the kits. The PCR primer sequences were showed in Table 1. The colon contents of mice were taken under sterile conditions and quickly frozen in liquid nitrogen for later use. Equal amounts of purified amplicon were pooled for subsequent sequencing. Total protein was isolated from the brain tissues using the protein extraction kit Solarbio, Beijing, China and adjusted to the same final concentration according to the BCA Assay Kit Beyotime Institute of Biotechnology, Shanghai, China. The membranes were washed three times in PBST buffer and incubated with a commercial western immunoblotting detection reagent western blue stabilized substrate for alkaline phosphatase, Promega, USA for 5 min. The resulting immunoreactive bands were exposed by Amersham Imager GE. Statistical analyses were performed using GraphPad Prism version 8. Shapiro—Wilk test was used to test normal distribution. The Kruskal—Wallis test was used when the variances were not homogeneous. We assessed correlations using Spearman's correlation coefficient. The contents of each main constituent were shown in Table 2. The main functional components of AS extract was protocatechuic acid 0. The polysaccharide was 6. The flavonoids 0. HPLC chromatogram and total ion chromatogram of Acanthopanax senticosus extract. As the results are shown in Table 3. The retention time of protocatechuic acid was 4. A square water maze was used to investigate the learning and memory abilities of irradiated mice. This trend showed that the effect of AS extract on preventing learning and memory impairment in irradiated mice became more significant with the increase in intervention days. The effect of AS extracts on behavioral performance. A The water maze design. B the platform arrival time. C the number of times to blind zones. D the sugar preference. Because rodents are extremely sensitive to sweet solutions, which serve as an effective reward for mice, sugar water preference is commonly used to assess the degree of hedonic loss. As shown in Figure 2D , radiation caused anhedonia in mice. HE staining results showed abnormal morphology of hippocampal neurons after radiation, with reduced cell volume, nucleus pyknosis, disordered arrangement, and loose structure Figure 3. AS extract alleviated the brain injury of irradiated mice. The functional integrity of the hippocampus includes not only the structural integrity but also the interaction of various neurotransmitters. The neurotransmitters in the hippocampus include monoamine neurotransmitters, cholinergic neurotransmitters and amino acid neurotransmitters, the synthesis process and content of which are related to the learning and memory of animals. We investigated potential changes in concentrations of neurotransmitters across the seven groups. GABA is the most widely distributed inhibitory neurotransmitter in the central nervous system, which is formed by the removal of the carboxyl group of the excitatory neurotransmitter glutamate in the brain under the action of glutamate decarboxylase GAD. The supplementation of AS extract changed the levels of neurotransmitters in the hippocampus. Intestinal motor function is mainly regulated by the local enteric nervous system ENS , and the lack or dysfunction of ENS can lead to intestinal dysfunction. In recent years, systematic studies on ENS have proved that there were many neurotransmitters in the gastrointestinal intermuscular plexus and submucosal plexus, which regulated the secretion and motility of the gastrointestinal tract. However, AS intervention changed the content of neurotransmitters in the colon. There was no obvious change in NE. It suggested that AS may affect the changes of neurotransmitters by changing the intestinal endocrine and movement. Given that the gut microbiota was also closely related to neurotransmitters, we next analyzed the changes in the gut microbiota. The supplementation of AS extract changed the levels of colonic neurotransmitters. At the phylum level, the domain bacteria were Bacteroidetes , Firmicutes , Proteobacteria , and Deferribacteres Figure 6A. Radiation reduced the relative abundance of Bacteroides , Lactobacillus. Meanwhile, PCoA results showed that the four groups of samples were separated from each other, which also proved that the addition of AS extract changed the composition of intestinal microbiota in mice Figure 6C. Lefse analysis was performed to find the key bactreia after radiation and AS extract intervention. AS extract reshaped the gut microbiota composition. A The relative abundance of bacteria at the phylum level. B The relative abundance of bacteria at the genus level. D Linear discriminant analysis LDA effect size shows the most differentially significant abundant taxa enriched in microbiota from the Model vs. Studies have shown that the synthesis of some neurotransmitters is closely related to gut microbiota. The results are shown in Figure 7. Correlation analysis among the gut microbiota and neurotransmitters. The size of the circle and the color shade represent the value of the correlation coefficient R. The larger the circle and the larger the R. We then detected the mRNA expression of colonic inflammatory factors and tight junction proteins. It is also one of the reasons for the changes in the intestinal microbiota. In addition, we detected the levels of inflammatory factors in the serum. AS extract prevented inflammation levels and colonic mucosa barrier impairment in irradiated mice. A The level of Inflammatory cytokines in serum. B The mRNA expression of inflammatory cytokines in the colon. C The mRNA expression of tight junction proteins in the colon of mice. Now the expression of BDNF at the protein level in the hippocampus was examined. AS extract supplementation may improve learning and memory ability by increasing the expression of BDNF. A The image of protein bands. The results are shown in Figure 10A. AS supplementation inhibited neuroinflammation. A The relative expression of inflammatory cytokines in the brain. The brain is highly sensitive to radiation, which usually causes a decline in learning and memory. This study mainly explored the protective effect of As extract on learning and memory impairment in irradiated mice under different days of dietary intervention. Many natural products are known for be radiation resistant, such as polysaccharides, saponins, and flavonoids. The roots and stems of AS mainly include syringin, eleutheroside D,eleutheroside E, and isofraxidin. The leaves and fruit of AS mainly contain flavonoids, saponins and organic acids. Some other studies have also reported changes of neurotransmitters in the brain after taking Chinese herbal medicine. These chemical messengers have excitatory or inhibitory effects on neurons. In this experiment, we found that different dosing cycles affected neurotransmitter levels. The AS extract contains polysaccharides, flavonoids, saponins, amino acids, and so on. The active components can interact with intestinal microbiota and exert physiological activities. On the one hand, the gut microbiota can metabolize some active components into new metabolites to play a role. For example, flavonoids can be converted into phenolic acids by the action of intestinal microbiota through enzymatic, hydrolytic, and dehydroxylation reactions to improve bioavailability. Glycosides are not easily absorbed in the intestinal tract, but can be metabolized by intestinal microbiota to deglycosylate glycosides, thus improving bioavailability. Bifidobacterium , Lactobacillus , Lachnospira , and Enterococcus efficiently participated in the deglycosylation hydrolysis reaction of the glycosides, while Bacillus and Clostridium can further degrade the sapogenins. For example, polysaccharide components have a prebiotic effect, which can promote the growth of beneficial bacteria and the metabolites can inhibit the reproduction of harmful bacteria. Moreover, plant extracts restored the diversity of gut microbiota and enhanced the growth of beneficial bacteria such as Lactobacillus and Bifidobacterium. In our study, AS extract intervention increased the relative abundance of Lactobacillus. Thirdly, plant extracts protect the intestinal barrier function by regulating flora and preventing bacterial translocation. Together, these active ingredients can play a role by regulating the gut microbiota in both direct and indirect ways. In the present study, the supplementation of AS extract enhanced the intestinal barrier function Figure 8. The marker bacteria in the AS extract group played an important role in learning and memory ability. Probiotic mixtures of Lactobacillus and Bifidobacterium strains significantly improved spatial memory deficits in diabetic animals, 37 and Streptococcus supplementation restored learning memory deficits. In addition, we speculated that the neurotransmitter changes induced by the intervention of AS extract may be closely related to the altered gut microbiota. The gut flora digests the host's dietary components while providing the host with energy and nutrients. The gut microbiota also produces some neuroactive metabolites, which can cause changes in neurotransmitters or their precursors. But the level of GABA decreased. Since neurotransmitters cannot directly penetrate the blood—brain barrier, 48 we speculated that the changes in neurotransmitters caused by AS were due to bacterial synthesis of neurotransmitters on the one hand, and neurotransmitter precursor substances produced by microbial metabolites to enter the blood—brain barrier on the other hand. Some studies have confirmed that metabolites or molecules of gut microbiota can travel up the vagus nerve to the brain, but it is unclear whether neurotransmitters produced in the gut can be transported to the brain through the vagus nerve. In conclusion, Acanthopanax senticosus extracts caused changes in the composition of gut microbiota, while also changing neurotransmitters and there was a correlation between the two. In addition, the destruction of intestinal tight junctions and the increase of inflammatory factors can lead to changes in intestinal permeability and thus changes in the gut microbiota. In this study, the AS extract also had a good protective effect on the intestinal tract. At the same time, it can also reduce the inflammatory factors of serum. Microglia is the resident innate immune cells in the brain, which respond to various stimuli that trigger the release of proinflammatory factors that could potentially damage the brain. BDNF is considered as a possible biomarker to monitor the onset, progression and treatment of brain lesions. Given that AS extract reduced the level of inflammation and alleviated brain damage in irradiated mice, our future studies will focus on its interaction in regulating neurotransmitter and microglia activation and neuroinflammation. In summary, the current research suggested AS extract improved cognitive function in a novel way and found a link between gut microbiota and cognitive function via neurotransmitters. Furthermore, AS extract reduced the level of inflammation and our future studies can focus on its interaction in regulating neurotransmitter and microglia activation. CNS Neurosci Ther. The data that support the findings of this study are available from the corresponding author upon reasonable request. The original blots images can be available in the Figures S1 and S2. 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