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Bile Acids Malabsorption Is Associated with Diarrhea in Acute Phase of Colitis

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Bile Acids Malabsorption Is Associated with Diarrhea in Acute Phase of Colitis Canadian Journal of Physiology and Pharmacology Bile acids malabsorption is associated with diarrhea in acute phase of colitis Journal: Canadian Journal of Physiology and Pharmacology Manuscript ID cjpp-2018-0017.R3 Manuscript Type: Article Date Submitted by the 16-Oct-2018 Author: Complete List of Authors: Rui-gang, Hou; Shanxi Medical University, School of Pharmaceutical; Second Hospital of Shanxi Medical University Lei, Fan; Shanxi Medical University, School of Pharmaceutical; Second Hospital of Shanxi Medical University Jun-jin, Liu;Draft Shanxi Medical University, School of Pharmaceutical; Second Hospital of Shanxi Medical University, Department of Pharmacy Yao, Chen; Shanxi Medical University, School of Pharmaceutical; Second Hospital of Shanxi Medical University, Zhuang-peng, Chang; Shanxi Medical University, School of Pharmaceutical; Shanxi Medical University, School of Pharmaceutical Bei, Wu; Shanxi Medical University; Second Hospital of Shanxi Medical University Yun-yun, Shao; Shanxi Medical University, School of Pharmaceutical; Second Hospital of Shanxi Medical University Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue: Keyword: colitis, bile acid malabsorption, ASBT, CYP7A1 https://mc06.manuscriptcentral.com/cjpp-pubs Page 1 of 37 Canadian Journal of Physiology and Pharmacology Title page Bile acids malabsorption is associated with diarrhea in acute phase of colitis Rui-gang Hou1,2, Lei Fan1,2, Jun-jin Liu1,2, Yao Cheng1,2, Zhuang-peng Chang1,2, Bei Wu1,2, Yun-yun Shao1,2* 1School of Pharmaceutical, Shanxi Medical University, Shanxi 030000 China 2Department of Pharmacy, Second Hospital of Shanxi Medical University, Shanxi 030000, China *Correspondence to: Draft Yun-yun Shao Department of Pharmacy, Second Hospital of Shanxi Medical University, Shanxi 030000, China Tel: +86 0351-3365405 Fax: +86-931-3365729 E-mail: [email protected]; [email protected] Yun-yun Shao Address: Department of Pharmacy, Second Hospital of Shanxi Medical University, No.382 Wuyi Road, Xinghualing District, Taiyuan City, Shanxi Province, 030000, China https://mc06.manuscriptcentral.com/cjpp-pubs Canadian Journal of Physiology and Pharmacology Page 2 of 37 Title page Draft https://mc06.manuscriptcentral.com/cjpp-pubs Page 3 of 37 Canadian Journal of Physiology and Pharmacology Manuscript Abstract The enterohepatic circulation of bile acids (BAs) critically depends on BA transporters and enzymes, which can be affected by inflammatory bowel disease. Diarrhea in colitis is believed to result in part from BA malabsorption (BAM). The work aimed to investigate whether diarrhea in colitis was associated with the expression of BA transporters, enzymes and nuclear receptors. RT-qPCR and Western blot techniques were used to evaluate the gene and protein levels of Cyp7a1, Asbt, SHP, FXR, Ostβ in a 2,4,6-trinitrobenzenesulfonic acid-induced rat model of colitis. The total bile acids (TBAs) levels were assayed using ELISA kits, and the individual BAs were measured by LC-MS/MS. Results showed that the fecal excretions of TBAs were significantly increased by 1.6-fold in acute stage of colitis. In ileum, Asbt was significantly decreased, however, Cyp7a1 level in liver wasDraft compensatory increased. Moreover, FXR has a decreased tendency and the downstream target gene SHP was downregulated. Contrary to acute stage, molecular changes were completely reversible during the remission phase. Our results indicated that the expression of Asbt and Cyp7a1 were altered in acute of colitis, which performed vital roles in maintaining BAs homeostasis. Early medical manipulation of BA transporters and enzymes may help prevent diarrhea. Key Words: colitis; bile acid malabsorption; ASBT; CYP7A1;FXR Abbreviations: BAM: bile acid malabsorption; TBAs: total bile acids; 5-HT: 5-hydroxytryptamine; TCA: taurocholate acid; TDCA: taurocheno deoxycholate acid; LCA: lithocholic acid; GCA: glycocholate acid; CA: cholic acid; CDCA: chenodeoxycholic acid; DCA: deoxycholic acid; NRs: nuclear receptors; CYP7A1: cholesterol 7a-hydroxylase; SHP: small heterodimerizing partner; ASBT: apical sodium-dependent bile acid transporter; NTCP: Na+/taurocholate co-transportingpoly peptide; OATPs: organic anion transporting polypeptides; BSEP: bile salt export pump; https://mc06.manuscriptcentral.com/cjpp-pubs Canadian Journal of Physiology and Pharmacology Page 4 of 37 Manuscript MRP2: multidrug-resistance protein 2; OSTα/β: organic solute transporter α/β; FXR: farnesoid X receptor; CAR: constitutive androstane receptor; HNF1: hepatocyte nuclear factor1; PPARγ: peroxisome proliferator-activated receptor gamma; TNBS: Trinitrobenzene sulfonic acid. Draft https://mc06.manuscriptcentral.com/cjpp-pubs Page 5 of 37 Canadian Journal of Physiology and Pharmacology Manuscript 1 Introduction 2 Inflammatory bowel diseases (IBD) are chronic recurrent inflammatory diseases of the 3 gastrointestinal tract, mainly including Crohn’s disease (CD) and ulcerative colitis (UC) 4 (Scharl et al. 2012). The incidence of IBD is increasing each year, while the 5 etiopathogenesis is still not fully understood (Burisch et al. 2013). IBD usually leads to 6 severe complications including pain, fatigue and weight loss. Persistent chronic diarrhea 7 is regarded as the more frequently complications even after the infection and associated 8 inflammation resolves. Prior observational studies have suggested a link between fluid 9 and ion transport and chronic diarrhea (Kalia N et al. 2007; Wenzl et al. 2012). A 10 common but frequently under investigated cause of chronic diarrhea is bile acid 11 malabsorption (BAM), resulting from dysregulation of the enterohepatic recycling of bile 12 acids and of bile acid production (VítekDraft et al. 2015; Camilleri et al. 2009). 13 14 Bile acids are amphiphilic molecules synthesized from cholesterol and play important 15 roles in lipid digestion and absorption (Cao et al. 2017; Sara Balesariaa 2008; 16 Vijayvargiya et al. 2013). BA homeostasis is controlled by an elaborate network of 17 nuclear receptors (NRs), enzymes and transporters (Camilleri et al. 2015). Cholesterol 18 7a-hydroxylase (CYP7A1) is the rate-limiting enzyme of bile acid synthesis in liver. 19 CYP7A1 could be down-regulated by small heterodimerizing partner (SHP) in the liver 20 (Jahnel et al. 2014; Li et al. 2004; Cao and Xu 2017). Farnesoid X receptor (FXR; 21 NR1H4), a transcriptional regulator of numerous genes involved in maintaining bile acid 22 homeostasis, plays important roles in maintaining bile acid pool size (Cariello et al. 2017; 23 Cheng et al. 2015). Specifically, FXR induces the expression of SHP in the liver, which 24 will in turn inhibit gene transcription of CYP7A1 (Kong et al. 2012). In the hepatocytes, 25 Na+/taurocholate co-transporting polypeptide (NTCP) and the organic anion transporting 26 polypeptides (OATPs) are transporters expressed in hepatic cell membrane responsible 27 for the BAs uptake. After binding to a cytosolic bile acid binding protein, BAs are https://mc06.manuscriptcentral.com/cjpp-pubs Canadian Journal of Physiology and Pharmacology Page 6 of 37 Manuscript 28 secreted into the bile by the bile salt export pump (BSEP) and multidrug-resistance 29 protein 2 (MRP2)(Cheng et al. 2017; He et al. 2011). Bile acids are then delivered to the 30 intestinal lumen through bile ducts, about 95% of the BAs are absorbed by the apical 31 sodium-dependent bile acid transporter (ASBT; gene symbol Slc10a2) and secreted into 32 the portal circulation by the basolateral organic solute transporter alpha/beta (Ostα/β) 33 heterodimer. ASBT mediates the initial uptake of bile acids across the ileal enterocyte 34 apical brush border membrane (Xiao et al. 2017) and performs an essential role in 35 maintenance of cholesterol homeostasis. It was reported that loss-of-function mutations 36 in the ASBT gene was one cause of congenital form of BAM (Montagnani et al. 2001). 37 Down-regulation of ileal Asbt in mice was associated with irinotecan-induced BAM (Shi 38 et al. 2017). Therefore, those transporters and receptors played vital roles in maintaining 39 a balance between bile acid synthesis,Draft secretion and intestinal reabsorption. 40 41 In the normal physiological state, enterohepatic circulation was responsible for bile acid 42 homeostasis. However, under certain pathophysiological conditions, this homeostasis was 43 disturbed, resulting in BAM in ileum (Silvennoinen et al. 2015). Multiple studies 44 confirmed BAM was a common cause of diarrhea that occurs in a number of different 45 clinical contexts, including Crohn’s disease, post-infectious diarrhea, postgastrectomy 46 syndrome (Jahnel et al. 2014; Lenicek et al. 2011; Sara Balesariaa 2008). However, the 47 key BA transporters participating in diarrhea in colitis were not fully elucidated. Based 48 on above evidence, we investigate whether diarrhea in colitis rats has correlation with the 49 altered expression of BA transporters. In this present study, we performed comprehensive 50 analytical and biochemical studies to clarify the correlation between BAM and chronic 51 diarrhea in colitis rats. Moreover, the gene and protein levels of Cyp7a1, Asbt, FXR, SHP 52 and Ostα/β were also evaluated to clarify the underlying mechanism of diarrhea in colitis. 53 54 Materials and methods https://mc06.manuscriptcentral.com/cjpp-pubs Page 7 of 37 Canadian Journal of Physiology and Pharmacology Manuscript 55 Materials 56 Taurocholate (TCA), taurochenodeoxycholate (TDCA), lithocholic acid (LCA), 57 glycocholate
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