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Determination of the Protective Effects of Hua‐Zhuo‐Jie‐Du in Chronic

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Determination of the Protective Effects of Hua‐Zhuo‐Jie‐Du in Chronic Zhou et al. Chin Med (2021) 16:37 https://doi.org/10.1186/s13020-021-00445-y Chinese Medicine RESEARCH Open Access Determination of the protective efects of Hua‐Zhuo‐Jie‐Du in chronic atrophic gastritis by regulating intestinal microbiota and metabolites: combination of liquid chromatograph mass spectrometer metabolic profling and 16S rRNA gene sequencing Pingping Zhou1, Xinyu Hao1, Yu Liu1, Zeqi Yang1, Miaochan Xu1, Shaowei Liu1, Shixiong Zhang1, Tianxiao Yang1, Xiaomei Wang1 and Yangang Wang1,2* Abstract Background: Hua-Zhuo-Jie-Du (HZJD), a Chinese herbal prescription consisting of 11 herbs, is commonly used in China to treat chronic atrophic gastritis (CAG). We aimed to determine the efect of HZJD on the microbiome-associ- ated metabolic changes in CAG rats. Methods: The CAG rat models were induced by 1-methyl-3-nitro-1-nitrosoguanidine (MNNG) combined with irregular fasting and 2% sodium salicylate, which was intragastrically administrated in fasted animals for 24 weeks. The CAG rats in the Chinese medicine (CM) group were administered a daily dose of 14.81 g/kg/day HZJD, and the vitacoenzyme (V) group were administered a daily dose of 0.08 g/kg/day vitacoenzyme. All animals were treated for 10 consecutive weeks, consecutively. Hematoxylin and eosin (H&E) staining was used to assess the histopathological changes in the gastric tissues. An integrated approach based on liquid chromatograph mass spectrometer (LC-MS) metabolic profling combined with 16S rRNA gene sequencing was carried out to assess the efects of HZJD on CAG rats. Spearman analysis was used to calculate the correlation coefcient between the diferent intestinal microbiota and the metabolites. Results: The H&E results indicated that HZJD could improve the pathological condition of CAG rats. The LC–MS results indicated that HZJD could signifcantly improve 21 gastric mucosal tissue perturbed metabolites in CAG rats; the afected metabolites were found to be involved in multiple metabolic pathways, such as the central carbon metabolism in cancer. The results of 16S rRNA gene sequencing indicated that HZJD could regulate the diversity, microbial composition, and abundance of the intestinal microbiota of CAG rats. Following HZJD treatment, the relative abundance of Turicibacter was increased, and the relative abundance of Desulfococcus and Escherichia were decreased in the CM group when compared with the M group. Spearman analysis revealed that perturbed intestinal *Correspondence: [email protected] 2 Beijing University of Chinese Medicine Third Afliated Hospital, Anwai Xiaoguan Street No. 51, Chaoyang District, 100029 Beijing, China Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zhou et al. Chin Med (2021) 16:37 Page 2 of 19 microbes had a strong correlation with diferential metabolites, Escherichia exhibited a negative correlation with l-Leucine, Turicibacter was negatively correlated with urea, and Desulfococcus exhibited a positive correlation with trimethylamine, and a negative correlation with choline. Conclusions: HZJD could protect CAG by regulating intestinal microbiota and its metabolites. Keywords: Hua‐Zhuo‐Jie‐Du, Chronic atrophic gastritis, LC–MS, 16S rRNA gene sequencing Background we constructed the “herb-compound-target-disease” Chronic atrophic gastritis (CAG) is a disease involving network diagrams, and found that 156 active ingredients chronic infammation of the gastric mucosa and is con- in HZJD had common targets with CAG [13]. Metabo- sidered to be an important precursor of gastric cancer. lomics is a systems biology approach that comprehen- Previous studies have shown that CAG is the most com- sively describes the pharmacological action of drugs and mon cause of cancer-related death and is ranked second the association between disease processes and specifc among other cancer-related causes of death worldwide biological pathways. Metabolomics has been increas- [1, 2]. CAG has increased in incidence because of various ingly applied to establish the therapeutic efect of TCM factors, such as eating habits, smoking [3], and microbial [16, 17] and has the potential to determine the novel infections [4]. Te treatment of CAG mainly involves regulatory mechanism of HZJD. Liquid chromatograph protecting the gastric mucosa, vitamin C supplementa- mass spectrometer (LC-MS) is an analytical method that tion, endoscopic minimally invasive treatment and eradi- is suitable for the separation and quantifcation of hard- cation of Helicobacter pylori [5–7]. Tese treatments, to-volatile compounds or compounds with poor thermal however, are often accompanied by adverse reactions [8]; stability. At present, the identifcation of metabolites has therefore, complementary and alternative intervention to been widely used in metabolomics research [18]. treat CAG are urgently required. At present, traditional Approximately 100 trillion gut microbes exist in the Chinese medicine (TCM) has been shown to be one of human body. Specifcally, the gut microbiota are com- the most promising methods for the treatment of CAG posed of large number of diferent bacteria that produce [9–12]. various metabolites and participate in important meta- In TCM, Hua-Zhuo-Jie-Du (HZJD) is a Chinese for- bolic functions, such as membraneand energy metabo- mula that is widely used in the treatment of CAG based lism [19, 20]. Accumulating evidence has shown that on the TCM theories of clearing away heat and damp- the gut microbiota contribute to the regulation of gas- ness, and removing turbidity and detoxifcation. HZJD trointestinal function [21]. Previous studies have shown consists of 11 herbs including Artemisia capillaris that the abundance of bacteria in patients with CAG is Tunb. (Yinchen), Scutellaria baicalensis Georgi (Huang- increased with the reduced secretion of gastric acid and qin), Coptis chinensis Franch. (Huanglian), Scutellaria that the changes in intestinal microbiota contribute to barbata D.Don (Banzhilian), Scleromitrion difusum the progression from intestinal metaplasia (IM) to gastric (Willd.) R.J.Wang (Baihuasheshecao), Isatis tinctoria L. cancer [22–24]. However, the association between the (Banlangen), Pogostemon cablin (Blanco) Benth. (Guang- metabolic phenotype and intestinal microbiota in CAG huoxiang), Lobelia chinensis Lour. (Banbianlian), Sophora and the changes noted during HZJD treatment of CAG favescens Aiton (Kushen), Eupatorium fortunei Turcz. remain unclear. (Peilan) and Gynostemma pentaphyllum (Tunb.) Mak- Te present study investigated the efect of HZJD on ino (Jiaogulan). Previous studies have reported on the the microbiome-associated metabolic changes in CAG possible mechanism of HZJD in the treatment of CAG, rats by employing an LC–MS-based metabolomics which is mainly suggested to be due to the regulation method coupled with 16S rRNA gene sequencing. To of cell proliferation and apoptosis [13, 14]. In a clinical the best of our knowledge, this is the frst study to exam- study, we compared the clinical efcacy, gastroscopic ef- ine the efect of HZJD on the intestinal microbiota and cacy and pathological efcacy of HZJD and ALaTanWu- metabolites of CAG rats. WeiWan for gastric precancerous lesions, and found that the efcacy of HZJD was better than the control group Materials and methods (P < 0.05), the mechanism was thought to be associated Preparation of HZJD with the decreased expression of HIF-1α, and VEGF and We prepared HZJD using the following procedure: the increased expression of PTEN [15]. TCM is a coordi- Artemisia capillaris Tunb. (Yinchen) 15 g, Scutel- nated system for the treatment of multitarget and mul- laria baicalensis Georgi (Huangqin) 12 g, Coptis chin- ticomponent diseases. In a network pharmacology study, ensis Franch. (Huanglian) 12 g, Scutellaria barbata Zhou et al. Chin Med (2021) 16:37 Page 3 of 19 D.Don (Banzhilian) 15 g, Scleromitrion difusum (Willd) analysis by 16S rRNA gene sequencing. Te stomach tis- R.J.Wang (Baihuasheshecao) 15 g, Isatis tinctoria L. (Ban- sues were divided into two parts on an ice tray; one part langen) 15 g, Pogostemon cablin (Blanco) Benth. (Guang- was immersed in paraformaldehyde (Servicebio, Wuhan, huoxiang) 9 g, Lobelia chinensis Lour. (Banbianlian) 15 g, China) for histological evaluation, and the other part was Sophora favescens Aiton (Kushen) 10 g, Eupatorium for- quickly stored at − 80 °C until required for analysis by tunei Turcz. (Peilan) 9 g and Gynostemma pentaphyllum LC–MS. (Tunb.) Makino (Jiaogulan)
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