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Research Article Perilla Oil Has Similar Protective Effects of Fish Oil on High-Fat Diet-Induced Nonalcoholic Fatty Liver Disease and Gut Dysbiosis

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Research Article Perilla Oil Has Similar Protective Effects of Fish Oil on High-Fat Diet-Induced Nonalcoholic Fatty Liver Disease and Gut Dysbiosis Hindawi Publishing Corporation BioMed Research International Volume 2016, Article ID 9462571, 11 pages http://dx.doi.org/10.1155/2016/9462571 Research Article Perilla Oil Has Similar Protective Effects of Fish Oil on High-Fat Diet-Induced Nonalcoholic Fatty Liver Disease and Gut Dysbiosis Yu Tian,1 Hualin Wang,1 Fahu Yuan,1,2 Na Li,1 Qiang Huang,1 Lei He,3 Limei Wang,1 and Zhiguo Liu1 1 School of Biology and Pharmaceutical Engineering, Wuhan Polytechnic University, Wuhan, Hubei 430023, China 2School of Medicine, Jianghan University, Wuhan, Hubei, China 3Department of Blood Transfusion, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China Correspondence should be addressed to Zhiguo Liu; zhiguo [email protected] Received 17 November 2015; Accepted 11 February 2016 Academic Editor: Dongmin Liu Copyright © 2016 Yu Tian et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Nonalcoholic fatty liver disease (NAFLD) is the most prevalent chronic liver disease in developed countries. Recent studies indicated that the modification of gut microbiota plays an important role in the progression from simple steatosis to steatohepatitis. Epidemiological studies have demonstrated consumption of fish oil or perilla oil rich in n-3 polyunsaturated fatty acids (PUFAs) protects against NAFLD. However, the underlying mechanisms remain unclear. In the present study, we adopted 16s rRNA amplicon sequencing technique to investigate the impacts of fish oil and perilla oil on gut microbiomes modification in rats with high- fat diet- (HFD-) induced NAFLD. Both fish oil and perilla oil ameliorated HFD-induced hepatic steatosis and inflammation. In comparison with the low-fat control diet, HFD feeding significantly reduced the relative abundance of Gram-positive bacteria in the gut, which was slightly reversed by either fish oil or perilla oil. Additionally, fish oil and perilla oil consumption abrogated the elevated abundance of Prevotella and Escherichia in the gut from HFD fed animals. Interestingly, the relative abundance of antiobese Akkermansia was remarkably increased only in animals fed fish oil compared with HFD group. In conclusion, compared with fish oil, perilla oil has similar but slightly weaker potency against HFD-induced NAFLD and gut dysbiosis. 1. Introduction caloric consumption, adipose tissue lipolysis activation, and hepatic insulin resistance all contribute to hepatic steatosis, Nowadays, overnutrition has become a big problem of human while gut-source endotoxins and proinflammatory cytokines health. Modern gastronomy encourages people to consume are associated with hepatic inflammation [4]. sugars, fats, and proteins more than needed, which lead to Recent studies have pointed out that intestinal microbiota caloric surplus and a series of metabolic diseases, such as playsacrucialroleinboth“hits”ofNAFLD[5].Intestinal nonalcoholic fatty liver disease (NAFLD) [1]. NAFLD, which microbiota, including bacteria, archaea, fungi, and viruses, characterises a spectrum of hepatic disorders range from contains almost 150-fold of DNA sequences than host [6]. simple steatosis to nonalcoholic steatohepatitis (NASH), is Intestinal microbiota affects the progress of NAFLD in two the most common cause of chronic liver diseases in developed major ways. (1) Gut bacteria affect nutrient digestion and countries [2]. A “two-hit” hypothesis has been used to explain absorption and produce secondary products such as medium the pathophysiology of NAFLD: the first hit, fat ectopic and short-chain fatty acids [7, 8]. Moreover, intestinal micro- accumulation in liver (steatosis), results in liver sensitive to biota influences host energy homeostasis; transplanting gut hepatic oxidative stress and inflammation, known as the sec- microbiota from obese mice induces body weight elevation in ond hit and leads to NASH [3]. Hyperphagia related excessive germ-free mice [9]. Another gut microbiota transplantation 2 BioMed Research International study illustrates its capability to regulate the expression of study was conducted according to the Guidelines for the hepatic genes for de novo lipogenesis [10]. Furthermore, Care and Use of Experimental Animals, and the protocol was gut microbiota affects the secretion of gut hormones, such approved by Laboratory Animal Ethics Committee of Wuhan as gastric inhibitory peptide, glucagon-like peptide 1, and Polytechnic University (ID number: 20121009006). At the end peptide YY, which contributes to the metabolic modification of16thweeksfeeding,12hoursfastedratsweresacrificedwith [11]. (2) Gut microbiota is closely related to host immune CO2 suffocate. Blood was then distributed into a heparinized ∘ system and hepatic inflammation. Gut Gram-negative bacte- tube (6–8 mL) and centrifuged at 1,000 g for 15 min at 4 C, ∘ ria are the major source of plasma lipopolysaccharide (LPS). and plasma was collected and stored at −80 Cuntilanalysis. Saturated fatty acids-enriched high-fat diet (HFD) induced Liver was quickly removed, rinsed with 0.9% sodium chloride endotoxemia leads to obesity and hepatic insulin resistance solution and weighed; a portion of the right hepatic lobe was ∘ and partly contributes to the death of gut Gram-negative either frozen in liquid nitrogen and kept at −80 C, or fixed in bacteria such as Bacteroides [12, 13]. The HFD also reduces the 10% neutral buffered formalin and embedded in paraffin for population of bifidobacteria in intestinum, thereby reducing histological studies. mucosal barrier and increasing intestinal permeability for translocation of gut LPS into plasma [12, 14, 15]. Besides, LPS 2.2. Measurement of Serum Parameters. Serum total choles- and gut bacteria can activate hepatic stellate cells and Kupffer terol (TCH), triglyceride (TG), low-density lipoprotein cells to induce liver fibrosis, a process that Toll-like receptors cholesterol(LDL-C),andtheactivityofserumalanine (TLRs) such as TLR5 and TLR9 may be involved [16–18]. aminotransferase (ALT) were determined using respective N-3 polyunsaturated fatty acids (PUFAs) are believed to diagnostic kits (Jiancheng Technology, Nanjing, China) have benefits against NAFLD [19]. n-3 PUFAs may attenuate according to the manufacturer’s instructions. All parameters the progress of NAFLD via either regulating lipid metabolism were measured in duplicate. or alleviating hepatic inflammation; both are associated with the function of gut microbiota [20]. Intestinal microbiota has 2.3. Histological Studies. The fixed liver tissues were embed- beenshowntocontributetotheeffectsofpalmoilinduced ded in paraffin and sectioned at 5 m thickness, stained with hepaticsteatosis[21].However,theinfluenceofn-3PUFAson hematoxylin and eosin. The stained slides were observed gut microbiota in the development of NAFLD is still unclear. photomicrographically, and the degree of liver steatosis was There are several kinds of n-3 PUFAs: docosahexaenoic acid examined blindly under a Nikon N80i microscope. (DHA, 22:6(n-3)) and eicosapentaenoic acid (EPA, 20:5(n- 3)), which are common in deep sea fish oil, and alpha- 2.4. Hepatic RNA Extraction and Quantitative RT-PCR. Total linolenic acid (ALA, 18:4(n-3)), which is common in particu- hepatic RNA was isolated from liver tissue using the TRI- lar plant oils, such as perilla oil. The different effects between ZOL reagent following supplier’s protocol (Takara, Dalian, n-3 ALA and DHA or EPA against NAFLD remain unknown. China). RNA quantity and quality were determined using the In the present study, we illustrated that n-3 PUFAs induced Nanodrop ND-1000 spectrophotometer (Thermo Fisher Sci- intestinal microbiome alteration at least partly contributes to entific) at a wavelength of 260/280 nm. cDNA was generated the amelioration of high-fat induced NAFLD, and perilla oil from 5 g of total RNA using M-MLV reverse transcriptase. A is as potent as fish oil. 20 L amplification reaction consisted of SYBR Green I PCR Master Mix (Takara, Dalian, China) with 300 nM of both 2. Method reverse and forward primers. All reactions were performed on a 7500 Real-time PCR System (Applied Biosystems). The ∘ 2.1. Animals and Diets. Male Sprague-Dawley (S-D) rats thermal cycling conditions were 2 min at 50 C, and 3 min at ∘ ∘ ∘ (8-9 weeks old weighing 180∼200 g) were purchased from 95 C, followed by 40 repeats at 95 Cfor15s,60Cfor30s, ∘ TonjiMedicalCollegeatHuazhongUniversityofScience and 72 C for 30 s. The fluorescent products were detected andTechnology(Wuhan,China).Theywerehousedfiveper atthelaststepofeachcycleinthereactions.Tocontrol cage and maintained in a 12-hour light/dark cycle under for variations in the reactions, the amount of target mRNA ∘ standard laboratory settings with a room temperature of 22 C was normalized to invariable control gene glyceraldehyde-3- ∘ ± 1 C, relative humidity of 60% ± 10%, and 20 air changes phosphate dehydrogenase (Gapdh) expression. The compar- per hour. After one week acclimation to the lab conditions, ative threshold cycle (Ct) method was used to determine the the rats were randomly allocated to four groups (10 animals amount of target gene normalized to Gapdh and relative to a −ΔΔCt per group), and each group was fed one of the following three calibrator 2 .ThepurityofPCRproductswasverifiedby diets for 16 weeks: normal chow diet with 10 kcal% fat (NOR melting curves and gel electrophoresis. group), Western
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