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Oral Administration of Compound Probiotics Ameliorates HFD Probiotics and Antimicrobial Proteins https://doi.org/10.1007/s12602-017-9378-3 Oral Administration of Compound Probiotics Ameliorates HFD-Induced Gut Microbe Dysbiosis and Chronic Metabolic Inflammation via the G Protein-Coupled Receptor 43 in Non-alcoholic Fatty Liver Disease Rats Yinji Liang1 & Shu Liang2 & Yupei Zhang2 & Yuanjun Deng2 & Yifang He2 & Yanning Chen2 & Chan Liu3 & Chenli Lin3 & Qinhe Yang2 # Springer Science+Business Media, LLC, part of Springer Nature 2018 Abstract The aim of this study was to investigate how the effects of compound probiotics modulate the gut microbiota, short-chain fatty acid (SCFA), body composition, serum and liver lipids, and inflammatory markers in non-alcoholic fatty liver disease (NAFLD) rats. Twenty-four male SD rats were randomly divided into 3 groups: normal control group (standard feed), high-fat diet (HFD) feeding group (83% standard feed + 10% lard oil + 1.5% cholesterol + 0.5% cholate + 5% sucrose), and compound probiotics intervention group (HFD + 0.6 g × kg−1 ×d−1 compound probiotics). The microbial population was assessed by 16S rDNA amplification and sequence analysis. Body composition, serum and liver lipids, serum inflammatory markers, colonic SCFAs, and relative proteins were assessed. The results showed that compound probiotics significantly reduced body weight, visceral and total fat mass, and the levels of hepatic TC and TG and serum TG, FFA, ALT, LPS, IL-1β, and IL-18 (P<0.05). The proportions of TM7 phylum (0.06 vs 1.57%, P<0.05) clearly increased, while that of Verrucomicrobia phylum (5.69 vs 2.61%, P<0.05) clearly decreased. Compound probiotics also increased the representation of Ruminococcus genus (0.95 vs 1.83%, P<0.05), while the proportion of Veillonella genus decreased (0.10 vs 0.03%, P<0.05). The levels of colonic SCFAs and GPR43, NLRP3, ASC, and CASPASE-1 proteins also changed significantly (P<0.05). Compound probiotics modulated gut microbiota, SCFAs, and their receptor GPR43 in NAFLD rats. These changes might inhibit lipid deposition and chronic metabolic inflammation in response to the insult of HFD. Keywords Non-alcoholic fatty liver disease . Probiotics . Gut microbiota . Inflammation . G protein-coupled receptor 43 Introduction has considered NAFLD to be a manifestation of metabolic syndrome in the liver, often associated with obesity, dyslipid- At present, non-alcoholic fatty liver disease (NAFLD) is emia, and insulin resistance [2]. According to the latest statis- among the most common liver diseases affecting the health tics, the incidence of NAFLD in adults was approximately of both adults and children worldwide [1]. Modern medicine 25.24% (N = 8,515,431) worldwide [3], and the number of cases was approximately 1 billion [4], approximately 30– Electronic supplementary material The online version of this article 40% in men and 15–20% in women [5]. The incidence of (https://doi.org/10.1007/s12602-017-9378-3) contains supplementary NAFLD in China was 15 to 30% [6], and the trend was in- material, which is available to authorized users. creasing annually. Increasing evidence suggests that NAFLD was a multisys- * Qinhe Yang tem disease. In addition to the progression of end-stage liver [email protected] disease, NAFLD is also closely related to many diseases, such 1 School of Nursing, Jinan University, No. 601 Huangpu Avenue West, as cardiovascular disease (CVD), type 2 diabetes mellitus Guangzhou, Guangdong 510632, China (T2DM), chronic kidney disease (CKD), and cancer [7]. 2 School of Traditional Chinese Medicine, Jinan University, No. 601 More than 70% of T2DM patients have been found to have Huangpu Avenue West, Guangzhou, Guangdong 510632, China NAFLD [8, 9]. A recent meta-analysis showed that the total 3 School of Basic Medicine, Jinan University, No. 601 Huangpu mortality of NAFLD increased by 57% due to NAFLD- Avenue West, Guangzhou, Guangdong 510632, China related CVD [10]. In addition, NAFLD increases the Probiotics & Antimicro. Prot. incidence and severity of CKD [11]. A comprehensive under- chain fatty acid (SCFA) production, and G protein-coupled standing of the harm to human health caused by NAFLD has receptor 43 (GPR43) in NAFLD rats. been obtained. However, the effective prevention and treat- ment of NAFLD in clinical practice remain lacking, and re- search on the pathogenesis of NAFLD is particularly urgent. Materials and Methods Recent research has led to widespread acceptance of the Bmultiple hit^ hypothesis regarding the pathogenesis Animals and Dietary Treatments of NAFLD [12]. The multiple hit factors mainly refer to the interaction of host genes, the environment (especially Twenty-four male Sprague Dawley rats (6 weeks old) were diet), and intestinal microorganisms, which could lead to obtained from the Laboratory Animal Research Center of gut microbiota dysbiosis, cause intestinal mucosa barrier Guangzhou University of Traditional Chinese Medicine dysfunction, and induce the translocation of the gut mi- (Animal License No. SCXK (Yue) 2013-0034). The basic diet crobiota and its metabolites [13, 14]. These factors inter- and high-fat diet (HFD) were provided, respectively, by the act to cause liver fat degeneration and activate the innate Animal Administration Laboratory of Jinan University and immune system, especially Toll-like receptors (TLRs) and the Center of Laboratory Animal Science of Guangdong NOD-like receptors (NLRs), inducing inflammation, cell (License No. SCXK (Yue) 2013-0002). Compound probiotics death, or progressive liver damage [12]. Professor Jeffrey were provided by Professor Heping Zhang from Inner Gordon’s team conducted a study on gut microbiota that Mongolia Agricultural University [23]. After adaptive feeding confirmed gut microbiota imbalance to be closely related for 1 week, the rats were randomly divided into three groups to metabolic diseases such as malnutrition, obesity, and with 8 rats per group, namely, the normal control group (NC diabetes [15]. However, the composition of the gut micro- group), the high-fat diet feeding group (HFD group), and the bial population may change dynamically in different en- compound probiotics intervention group (CP group). This an- vironments, nutrition conditions, or immune states. In ad- imal experiment protocol was approved by the Laboratory dition, disorders of the gut microbiota exert a profound Animal Ethics Committee of Jinan University. NC group rats impact on the host health and a variety of diseases [16]. A were fed standard feed, and the other groups were fed a HFD randomized controlled trial showed that the populations of (83% standard feed + 10% lard oil + 1.5% cholesterol + 0.5% aerobic bacteria such as Enterobacteriaceae and cholate + 5% sucrose). At the same time, each rat was, respec- Enterococcus faecalis were significantly increased in pa- tively, given distilled water or the relevant medicine by ga- tients with NASH compared with the healthy control vage. The HFD group rats were given deionized distilled wa- group, while Lactobacillus, Bifidobacteria, and other an- ter, and the CP group rats were given compound probiotics aerobic bacteria were decreased [17]. The severity of (more than 600 billion CFU/100 g) at 0.6 g × kg−1 ×d−1.The NAFLD is also closely related to the abundance of γ- compound probiotics contained 9 strains of probiotics, includ- Proteus in the intestine [18]. Despite some controversial ing 6 strains of Lactobacillus and 3 strains of Bifidobacterium results, these studies indicated that certain specific phy- combined with 15 g/100 g of the prebiotic galacto- lum, class, order, family, genus, or species populations oligosaccharide (GOS). Composition of feed used in the study may be beneficial or harmful to NAFLD patients. was shown in Supplemental Table 1–3. Body weight and food Therefore, the regulation of the intestinal ecological bal- intake were measured weekly. The rats were allowed to drink ance may be an important means of preventing and water freely and were kept in separate cages in an SPF animal treating NAFLD. The intestinal ecological balance de- laboratory with 12-h alternating periods of dark and light at pends on the stability of the intestinal epithelial mucosa, 18–22 °C for 16 weeks. the gut microbiota, and the regulation of its metabolites. Recently, some studies found that the gut microbiota, as- Gut Microbiota Sequencing Analyses sociated high concentrations of intestinal SCFAs and G protein-coupled receptors (GPCRs), played a key role in At 1–2 days before euthanasia, fresh stool samples (n =8 NAFLD [19–22], but it remained unclear how the gut rats/group) were collected in sterile tubes and stored in liquid microbiota communicated with the liver. Thus, due to nitrogen. Fecal sample DNA was extracted with QiaAmp the close relationship between the liver and gut, the ques- DNA Mini Kits (Qiagen, Valencia, CA, USA), and the bacte- tion of whether compound probiotics could regulate the rial genomic DNA was detected by gel electrophoresis. The gut microbiota and its metabolites in NAFLD is worthy of sample DNA was amplified to enrich for the bacterial 16S further study. V3–V4 rDNA region with a specific primer with a barcode Our study investigated the effects of compound probiotics [ 24]. The primer sequences were 341F: on the gut microbiota and its impact on body composition, CCTAYGGGRBGCASCAG and 806R: serum and liver lipids, serum inflammatory markers, short- GGACTACNNGGGTATCTAAT. Then, the PCR Probiotics & Antimicro. Prot. amplification product was recovered and quantified using a mass, fat volume, average CT value, and fat ratio and can QuantiFluorTM fluorometer. The purified amplification prod- obtain the CT value ratio and the fat ratio of the liver to deter- ucts were mixed in equal amounts, ligated to sequencing mine the degree of deterioration of the fatty liver [26]. adapters to construct a sequencing library, and sequenced on a HiSeq2500 system using the PE250 run mode. For taxo- Biochemical Measurements in Serum and Hepatic nomic classification, tag reads were grouped into operational Tissue taxonomic units (OTUs) at a sequence similarity level of 97%.
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