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Original Article Glutamine with Probiotics Attenuates Intestinal Inflammation and Oxidative Stress in a Rat Burn Injury Model T

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Original Article Glutamine with Probiotics Attenuates Intestinal Inflammation and Oxidative Stress in a Rat Burn Injury Model T Am J Transl Res 2017;9(5):2535-2547 www.ajtr.org /ISSN:1943-8141/AJTR0048803 Original Article Glutamine with probiotics attenuates intestinal inflammation and oxidative stress in a rat burn injury model through altered iNOS gene aberrant methylation Zhen-Yu Gong, Zhi-Qiang Yuan, Zhi-Wei Dong, Yi-Zhi Peng State Key Laboratory of Trauma, Burns and Combined Injury, Institute of Burn Research, Southwest Hospital, The Third Military Medical University, Chongqing 400038, China Received January 13, 2017; Accepted May 1, 2017; Epub May 15, 2017; Published May 30, 2017 Abstract: Severe burns may lead to intestinal inflammation and oxidative stress resulting in intestinal barrier dam- age and gut dysfunction. In the management of severe burns, therapies are needed to attenuate whole-body inflam- matory responses and control the burden of oxidative stress. In this study, we evaluated the effects of oral gluta- mine (Gln) with probiotics on burn-induced intestinal inflammation and oxidative stress using a Wistar rat burn injury model. We then explored potential molecular mechanisms for the effects of glutamine and probiotics on intestinal tissue inflammation and oxidative stress. We found that glutamine and probiotics together significantly inhibited nitric oxide (NO) content; reduced levels of the inflammatory factors TNF-α, IL-6, and IL-8; and altered expression of oxidative stress factors including reactive oxygen species and superoxide dismutase. We found that the apoptotic proportion of intestinal epithelial cells in severely burned subjects was notably decreased following treatment with glutamine plus probiotics. We also found that glutamine and probiotics given together markedly reduced NO content by down-regulating the expression of iNOS in blood and intestinal tissue. These findings indicate that regulation of the iNOS gene plays a pivotal role in inflammation and oxidative stress in the response to severe burns in the Wistar rat. We then further investigated the mechanism by which combined therapy with glutamine and probiotics might reduce expression of iNOS and found that this treatment resulted in increased methylation of the iNOS gene. The methylation level of the iNOS gene was found to be regulated via differential expression of DNMT1 and Tet1. Collectively, our results suggest that combined therapy with glutamine and probiotics can markedly reduce the syn- thesis of NO, suppressing intestinal inflammation and oxidative stress in the Wistar rat burn injury model. Keywords: Glutamine, probiotics, NO, iNOS, DNA methylation Introduction thelial cells, leading to increased permeability of the mucosa and thereby permitting bacteria Severe burns can be associated with intestinal and other macromolecular substances to pass inflammation and oxidative stress which may into the bloodstream, causing additional oxida- then lead to intestinal barrier damage and fur- tive stress and provoking further inflammation. ther organ dysfunction [1-3]. The intestinal tract This cycle can cause progressive damage to the serves as the largest immune system organ in intestinal mechanical and immune barriers, the body. Thus, following severe burn injury, the eventually leading to worsening systemic infec- intestinal tract is the first organ to be damaged tion and inflammation if not controlled [6-8]. by associated systemic stress and inflamma- tion [4, 5]. Severe burns can directly and indi- A significant increase in intestinal tract nitric rectly lead to intestinal injury by contributing to oxide (NO) following burn injury has been previ- overgrowth of intestinal bacteria, compromis- ously reported in a rat severe burn injury model ing the integrity of the intestinal wall, and [9]. Under physiological conditions, NO is widely reducing immune system responsiveness. In distributed in gastrointestinal tract tissues, the setting of ongoing inflammation, apoptosis where this substance plays roles in peristalsis and necrosis may occur among intestinal epi- and mucosal protection [10, 11]. Following Glutamine and probiotics attenuate inflammatory response through iNOS severe burn injury, NO has been proposed to Jiangsu, China). Probiotics were purchased play an important role in the intestinal tract from Beijing Tongrentang Co., Ltd (X12-110, inflammatory response to injury [12, 13]. NO is Beijing, China). generated from L-arginine through a reaction catalyzed by nitric oxide synthase (NOS). NOS is Wistar rat burn injury model: model creation, known to have the forms neuronal NOS (nNOS), study groups, and data collection endothelial NOS (eNOS), and inducible NOS (iNOS) [14]. In response to a range of stimuli, 120 healthy male Wistar rats (4-6 weeks) from including pro-inflammatory factors, foreign anti- local experimental animal center in Southwest gens, lipopolysaccharide (LPS), and cytokine hospital were used in this study. Rats were stimulation, the expression of iNOS is upregu- obtained and then fed for one week. Subjects lated in macrophages, T lymphocytes, liver were randomly selected for inclusion in the cells, muscle cells, and endothelial cells; abun- severe burn group (n = 80). All rats were dant NO production can induce a severe inflam- weighed prior to burn injury creation or control matory response [15-17]. warm water treatment. Burn injuries were cre- ated by scalding the skin of the back using boil- Previous studies have found significantly ing water. Prior to burn creation, each rat decreased glutamine in muscle tissues and received an intraperitoneal injection of 3% plasma after severe burn injury [18]. Glutamine pentobarbital sodium (40 mg/kg) as an anes- supplementation has been found to promote thetic. The hair on each subject’s back was biological processes necessary for intestinal then removed using scissors. The analgesic repair, intestinal injury relief, maintenance of buprenorphine (1 mg/kg) was injected to pro- intestinal barrier functions, and prevention of vide pain relief. A custom-made positioning intestinal bacterial and endotoxin translocation apparatus was used to hold subjects while a [19-21]. In addition, probiotics, microbial prepa- scald burn injury was created on the back of rations containing physiologically active bacte- the animal. To create the burn injury, the test ria and their byproducts, have also been found area on the back was completely immersed in to inhibit the growth of pathogenic bacteria, boiling water (100°C) for 15 seconds (s), creat- reduce intestinal inflammation, and inhibit sig- ing a 20% body surface area full thickness naling pathways including the NF-κB pathway; burn. Rats in the normal control group were these activities may result in suppression of treated with warm water (25°C, 15 s) and other- inflammatory reactions, protection of intestinal wise received the same treatment as rats in epithelial cells, and enhancement of the intesti- the burn group. Following burn injury creation, nal mechanical barrier [22-24]. To achieve syn- animals were caged individually for 1 day, then ergistic benefits in the treatment of intestinal returned to their cages and permitted to eat injury following severe burns, glutamine and and drink freely. probiotics can be used together. However, the degree of synergy and the specific mechanisms Oral gavage was used to administer the follow- accounting for the combined effects of gluta- ing treatments to burn injury and control rats: mine and probiotics remain to be studied. control group (n = 15), 1 ml normal saline; burn model group (n = 15), 1 ml normal saline; gluta- In this investigation we evaluated the effects of mine treatment group (Gln group; n = 15), 1.5 glutamine combined with probiotics on intesti- g/kg glutamine + 1 ml normal saline; probiotics nal injury using a Wistar rat severe burn model. treatment group (probiotics group; n = 15), 300 The objectives of this study were to identify and mg/kg probiotic + 1 ml normal saline; gluta- characterize treatment effects and mecha- mine and probiotics combined treatment group nisms for further exploration in subsequent (n = 15), 1.5 g/kg + 300 mg/kg glutamine + 1 clinical trials in burn patients. ml normal saline. Treatments were given once Materials and methods per day for seven days. Wounds were treated with iodophor (Mosen disinfection technology Materials Co. Ltd, Shandong, China) each day. Wounds were kept dry and clean. And rats were treated L-glutamine was purchased from Jiangsu according to the following methods: subjects in Shenhua Pharmaceutical Co., Ltd (Z320210, the control group (n = 15) and the burn model 2536 Am J Transl Res 2017;9(5):2535-2547 Glutamine and probiotics attenuate inflammatory response through iNOS group (n = 15) were administered 1 ml saline cation (Leica DM1000, Leica, Wetzlar, Germany) by tail intravenous injection immediately after and photographed. injury. Rats in the L-NAME (N-nitro-L-arginine methyl ester, NOS-specific inhibitor, S0006, Blood sample biochemical index determination Beyotime Biotechnology, Shanghai, China) group (n = 15) received L-NAME HCL (100 mg/ IL-6, IL-4, IL-8 and TNF-α (ASS3189, ASS3182, kg) by tail intravenous injection immediately KHC0081 and KHC3012, Abgent, San Diego, after burn injury creation. CA, USA) were measured using ELISA assays. ROS (MAK144-1KT, Sigma-Aldrich, St. Louis, Blood and tissue samples were collected after MO, USA) and SOD (19160-1KT-F, Sigma- three and seven days of treatment. Subjects Aldrich, St. Louis, MO, USA) were measured were weighed and then anesthetized using an using chemiluminescent assays. NO was mea- intraperitoneal
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