Polygonum tinctorium leaves suppress sodium dextran sulfate-induced colitis through interleukin-10-related pathway

Taka Asari; Hidezumi Kikuchi; Shogo Kawaguchi; Hirotake Sakuraba; Shukuko Yoshida; Yui Akemoto; Takato Maeda; Ota Shinji; Yasuhisa Murai; Naoki Higuchi; Kentaro Hoshi; Yukari Fukutoku; Hiroto Hiraga; Kenroh Sasaki; Shinsaku Fukuda

doi:10.1016/j.bbrep.2022.101272

Polygonum tinctorium leaves suppress sodium dextran sulfate-induced colitis through interleukin-10-related pathway

Biochem Biophys Rep. 2022 May 2:30:101272. doi: 10.1016/j.bbrep.2022.101272. eCollection 2022 Jul.

Authors

Affiliations

¹ Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, 5-Zaifu-cho, Hirosaki, Aomori, 036-8562, Japan.
² Department of Community Medicine, Hirosaki University Graduate School of Medicine, 5-Zaifu-cho, Hirosaki, Aomori, 036-8562, Japan.
³ Department of Vascular Biology, Hirosaki University Graduate School of Medicine, 5-Zaifu-cho, Hirosaki, Aomori, 036-8562, Japan.
⁴ Shibata Irika Co. Ltd., 3-7-1-Takada, Hirosaki, Aomori, 036-8084, Japan.
⁵ Department of Anatomic Pathology, Hirosaki University Hospital, 53-Honcho, Hirosaki, Aomori, 036-8563, Japan.
⁶ Division of Pharmacognosy, Tohoku Medical and Pharmaceutical University, 4-4-1- Komatsushima, Aobaku, Sendai, Miyagi, 981-8558, Japan.

Abstract

Indigo naturalis, a herbal medicine purified from indigo-containing plants, such as Strobilanthes cusia, Isatis tinctoria, and Polygonum tinctorium, has been reported to be useful in the treatment of ulcerative colitis by activating the aryl hydrocarbon receptor. However, the aryl hydrocarbon receptor pathway causes crucial side effects, such as pulmonary arterial hypertension. Although P. tinctorium is one of the plant derivatives of indigo naturalis, it is not identical to it. To date, the pure leaves of P. tinctorium have not been reported to ameliorate ulcerative colitis. Therefore, we investigated the effect of pure P. tinctorium leaves, which are consumed in some regions, on experimental colitis induced in mice using sodium dextran sulfate. We found that P. tinctorium leaves ameliorated weight loss (P < 0.01) and pathological inflammatory changes in the colon (P < 0.05), enhanced mRNA expression of interleukin-10 (P < 0.05), and decreased expression of tumor necrosis factor-in colonic tissues (P < 0.05), as determined using quantitative real-time reverse transcription polymerase chain reaction. The intraperitoneal administration of an aryl hydrocarbon receptor antagonist did not antagonize the inhibition of mucosal destruction, whereas an anti-interleukin-10 receptor antibody did. These results suggest that P. tinctorium ameliorate sodium dextran sulfate-induced intestinal inflammation via interleukin-10-related pathway, independent of the aryl hydrocarbon receptor pathway. P. tinctorium leaves have the potential to be a new, safe treatment for ulcerative colitis.

Keywords: AhR, aryl hydrocarbon receptor; Aryl hydrocarbon receptor pathway; CD, Crohn's disease; DSS, sodium dextran sulfate; EDTA, ethylenediaminetetraacetic acid; H & E, hematoxylin and eosin; HBSS, Hank's balanced salt solution; HPLC, high performance liquid chromatography; IBD, inflammatory bowel disease; IECs, intestinal epithelial cells; IFN, interferon; IL, interleukin; Indigo naturalis; Interleukin-10; LP, lamina propria; PAH, pulmonary arterial hypertension; Polygonum tinctorium; SEM, standard error of the mean; TGF, transforming growth factor; TNF, tumor necrosis factor; UC, ulcerative colitis; qRT-PCR, quantitative real-time reverse transcription polymerase chain reaction; ulcerative Colitis.