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Daikenchuto (Da-Jian-Zhong-Tang) Ameliorates Intestinal Fibrosis by Activating Myofibroblast Transient Receptor Potential Ankyrin 1 Channel

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Daikenchuto (Da-Jian-Zhong-Tang) Ameliorates Intestinal Fibrosis by Activating Myofibroblast Transient Receptor Potential Ankyrin 1 Channel Submit a Manuscript: http://www.f6publishing.com World J Gastroenterol 2018 September 21; 24(35): 4036-4053 DOI: 10.3748/wjg.v24.i35.4036 ISSN 1007-9327 (print) ISSN 2219-2840 (online) ORIGINAL ARTICLE Basic Study Daikenchuto (Da-Jian-Zhong-Tang) ameliorates intestinal fibrosis by activating myofibroblast transient receptor potential ankyrin 1 channel Keizo Hiraishi, Lin-Hai Kurahara, Miho Sumiyoshi, Yao-Peng Hu, Kaori Koga, Miki Onitsuka, Daibo Kojima, Lixia Yue, Hidetoshi Takedatsu, Yu-Wen Jian, Ryuji Inoue Keizo Hiraishi, Lin-Hai Kurahara, Miho Sumiyoshi, Yao-Peng and No. 25860571; a MEXT-Supported Program supporting research Hu, Ryuji Inoue, Department of Physiology, Graduate School of activities of female researchers; the Clinical Research Foundation; Medical Sciences, Fukuoka University, Fukuoka 8140180, Japan and the Central Research Institute of Fukuoka University, No. 151045 and No. 147104. Kaori Koga, Miki Onitsuka, Department of Pathology, Faculty of Medicine, Fukuoka University, Fukuoka 8140180, Japan Institutional review board statement: The study was reviewed and approved by the Clinical Research Ethics Committee of Daibo Kojima, Department of Gastroenterological Surgery, Faculty Fukuoka University, No. 15-10-04. of Medicine, Fukuoka University, Fukuoka 8140180, Japan Institutional animal care and use committee statement: All Lixia Yue, Department of Cell Biology, University of Connecticut procedures involving animals were reviewed and approved by Health Center, Farmington, CT 06030, United States the Animal experiment ethics committee of Fukuoka University, No. 1709099; and the Genetic Modification Experiment Safety Hidetoshi Takedatsu, Department of Gastroenterology and Commission of Fukuoka University approved experiments on Medicine, Faculty of Medicine, Fukuoka University, Fukuoka genetically modified animals, No. 167. 8140180, Japan Conflict-of-interest statement: The authors declare that they Yu-Wen Jian, College of Letters and Science, University of have no competing interests. California, Davis, CA 95616, United States Data sharing statement: Readers can request the data of this ORCID number: Keizo Hiraishi (0000-0002-2050-1721); paper by contacting us via [email protected]. Lin-Hai Kurahara (0000-0001-7425-5768); Miho Sumiyoshi (0000-0002-0264-3689); Yao-Peng Hu (0000-0002-0893-2705); ARRIVE guidelines statement: The authors have read the Kaori Koga (0000-0001-7103-242X); Miki Onitsuka ARRIVE guidelines, and the manuscript was prepared and revised (0000-0002-2546-7091); Daibo Kojima (0000-0001-5388-8320); according to the ARRIVE guidelines. Lixia Yue (0000-0002-3558-091X); Hidetoshi Takedatsu (0000-0002-0318-0129); Yu-Wen Jian (0000-0003-4080-2879); Open-Access: This article is an open-access article which was Ryuji Inoue (0000-0002-8494-4900). selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Author contributions: Kurahara LH designed the experiments Commons Attribution Non Commercial (CC BY-NC 4.0) license, and wrote the paper, Hiraishi K, Kurahara LH and Sumiyoshi M which permits others to distribute, remix, adapt, build upon this performed most of the experiments and analyzed the data; Hu YP work non-commercially, and license their derivative works on conducted patch-clamp experiments and analyzed the obtained different terms, provided the original work is properly cited and data; Koga K and Onitsuka M performed the pathological the use is non-commercial. See: http://creativecommons.org/ analysis; Yue L provided comments; Kojima D and Takedatsu H licenses/by-nc/4.0/ gave clinical advice, recruited study participants, and performed the biopsies and surgical resections of tissue; Jian YW created the Manuscript source: Unsolicited manuscript graphical abstract; and Inoue R supervised the study and assisted in the preparation of the manuscript. Correspondence to: Lin-Hai Kurahara, PhD, Lecturer, Department of Physiology, Fukuoka University School of Medicine, Supported by MEXT, KAKENHI, No. 15K08978, No. 22790677 Fukuoka 8140180, Japan. [email protected] WJG|www.wjgnet.com 4036 September 21, 2018|Volume 24|Issue 35| Hiraishi K et al . Daikenchuto suppresses fibrosisvia TRPA1 activation Telephone: +81-92-8011011-3236 Key words: Intestinal fibrosis; Myofibroblast; Transient Fax: +81-92-8656032 receptor potential ankyrin 1; Crohn’s disease; Collagen; α-smooth muscle actin Received: May 16, 2018 Peer-review started: May 16, 2018 © The Author(s) 2018. Published by Baishideng Publishing First decision: June 13, 2018 Group Inc. All rights reserved. Revised: July 6, 2018 Accepted: July 22, 2018 Article in press: July 22, 2018 Core tip: Active ingredients of the famous Chinese Published online: September 21, 2018 medicine Da-Jian-Zhong-Tang (Daikenchuto; DKT), i.e. , hydroxy α-sanshool and 6-shogaol, induced Ca2+ influxes in intestinal myofibroblast (InMyoFib), which were antagonized by co-treatment with a selective transient receptor potential ankyrin 1 (TRPA1) channel Abstract blocker HC-030031. DKT counteracted the transforming AIM growth factor (TGF)-β1-induced expression of Type Ⅰ To investigate the anti-fibrotic effects of the traditional collagen, α-smooth muscle actin (α-SMA), and this was oriental herbal medicine Daikenchuto (DKT) associated accompanied by a reduction in fibrosis signaling down- with transient receptor potential ankyrin 1 (TRPA1) chan- stream of the TGF-β1 receptor. Importantly, a 24-h nels in intestinal myofibroblasts. incubation with another DKT active ingredient of Japanese Pepper increased mRNA and protein expression in TRPA1, METHODS which in turn negatively regulated collagen synthesis in Inflammatory and fibrotic changes were detected in a InMyoFibs. In stenotic regions of the intestines of patients 2,4,6-trinitrobenzenesulfonic acid (TNBS) chronic colitis with Crohn’s disease, TRPA1 expression was significantly model of wild-type and TRPA1-knockout (TRPA1-KO) increased. mice via pathological staining and immunoblotting ana- lysis. Ca2+ imaging experiments examined the effects of DKT and its components/ingredients on intestinal myo- Hiraishi K, Kurahara LH, Sumiyoshi M, Hu YP, Koga K, fibroblast (InMyoFib) cell TRPA1 channel function. Pro- Onitsuka M, Kojima D, Yue L, Takedatsu H, Jian YW, Inoue R. fibrotic factors and transforming growth factor (TGF)- Daikenchuto (Da-Jian-Zhong-Tang) ameliorates intestinal fibrosis β1-associated signaling were tested in an InMyoFib cell by activating myofibroblast transient receptor potential ankyrin line by qPCR and immunoblotting experiments. Samples 1 channel. World J Gastroenterol 2018; 24(35): 4036-4053 from non-stenotic and stenotic regions of the intestines Available from: URL: http://www.wjgnet.com/1007-9327/full/ of patients with Crohn’s disease (CD) were used for patho- v24/i35/4036.htm DOI: http://dx.doi.org/10.3748/wjg.v24. logical analysis. i35.4036 RESULTS Chronic treatment with TNBS caused more severe inflam- mation and fibrotic changes in TRPA1-KO than in wild-type INTRODUCTION mice. A one-week enema administration of DKT reduced Daikenchuto (DKT; Da-Jian-Zhong-Tang in Chinese) is fibrotic lesions in wild-type but not in TRPA1-KO mice. a traditional herbal medicine, originally described in Jin The active ingredients of DKT, i.e., hydroxy α-sanshool 2+ Gui Yao Lue (“Essential Prescriptions from the Golden and 6-shogaol, induced Ca influxes in InMyoFib, and this Cabinet”), a classic book of Chinese medicine published was antagonized by co-treatment with a selective TRPA1 more than 1800 years ago. DKT is often used for post- channel blocker, HC-030031. DKT counteracted TGF-β1- operative ileus and constipation, and is composed of induced expression of Type Ⅰ collagen and α-smooth muscle actin (α-SMA), which were accompanied by a several crude components, Zingiberis rhizoma (Ginger), reduction in the phosphorylation of Smad-2 and p38- Panax ginseng (Ginseng; Ginseng radix), Zanthoxyli mitogen-activated protein kinase (p38-MAPK) and the fructus (Japanese pepper), and malt sugar. DKT gene- expression of myocardin. Importantly, 24-h incubation rally accelerates gastrointestinal motility; it increases with a DKT active component Japanese Pepper increased intestinal blood flow and gastrointestinal hormone se- [1-3] the mRNA and protein expression levels of TRPA1 in cretion . Numerous basic studies have demonstrated InMyoFibs, which in turn negatively regulated collagen the effects of DKT on vasodilation, inflammation, and [4-9] synthesis. In the stenotic regions of the intestines of CD bacterial translocation . Ginger contains several active patients, TRPA1 expression was significantly enhanced. ingredients, such as gingerols and shogaols (6-, 8-, and 10- isomers), which have anti-inflammatory and CONCLUSION vasoprotective effects via modulating the activities of The effects of DKT on the expression and activation of the mitogen-activated protein kinase (MAPK), protein kinase TRPA1 channel could be advantageous for suppressing B (Akt), and NF-κB[10-12]. Japanese pepper contains intestinal fibrosis, and benefit inflammatory bowel disease hydroxy-α and hydroxy-β-sanshools that alter intestinal treatment. blood flow, motility, and barrier function by inducing the WJG|www.wjgnet.com 4037 September 21, 2018|Volume 24|Issue 35| Hiraishi K et al . Daikenchuto suppresses fibrosisvia TRPA1 activation synthesis/secretion of adrenomedullin and calcitonin CD4+-T cells into Th1-effector cells[32]. Finally, TRPA1 gene-related peptides[1,13]. DKT accelerates
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