Propionate ameliorates dextran sodium sulfate-induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stress

Propionate is a short chain fatty acid and abundant as butyrate in the gut and blood. However, propionate has been studied less extensively than butyrate in the treatment of colitis. The present study was to investigate the effects of sodium propionate on intestinal barrier function, inflammation an...

Full description

Bibliographic Details
Main Authors: Lingchang Tong, Yue Wang, Zhi-bin Wang, Wei-ye Liu, Sheng Sun, Li-chao Zhang, Ding-feng Su, LING LI
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-08-01
Series:Frontiers in Pharmacology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fphar.2016.00253/full
_version_ 1811256977852989440
author Lingchang Tong
Lingchang Tong
Yue Wang
Yue Wang
Zhi-bin Wang
Wei-ye Liu
Sheng Sun
Li-chao Zhang
Ding-feng Su
LING LI
author_facet Lingchang Tong
Lingchang Tong
Yue Wang
Yue Wang
Zhi-bin Wang
Wei-ye Liu
Sheng Sun
Li-chao Zhang
Ding-feng Su
LING LI
author_sort Lingchang Tong
collection DOAJ
description Propionate is a short chain fatty acid and abundant as butyrate in the gut and blood. However, propionate has been studied less extensively than butyrate in the treatment of colitis. The present study was to investigate the effects of sodium propionate on intestinal barrier function, inflammation and oxidative stress in dextran sulfate sodium (DSS)-induced mice. Animals in DSS group received drinking water from 1 to 6 days and DSS (3% (w/v) dissolved in double distilled water) instead of drinking water from 7 to 14 days. Animals in DSS+Prop group were given 1% sodium propionate for 14 consecutive days and supplemented with 3% DSS solution on day 7-14. Intestinal barrier function, proinflammatory factors, oxidative stress, and signal transducer and activator of transcription 3 (STAT3) signaling pathway in the colon were determined. It was found that sodium propionate ameliorated body weight loss, colon-length shortening and colonic damage in colitis mice. Sodium propionate significantly inhibited the increase of FITC-dextran in serum and the decrease of zonula occludens-1 (ZO-1), occludin and E-cadherin expression in the colonic tissue. It also inhibited the expression of interleukin (IL)-1β, IL-6 and tumor necrosis factor-α (TNF-α) mRNA and phosphorylation of STAT3 in colitis mice markedly, reduced the myeloperoxidase (MPO) level, and increased the superoxide dismutase (SOD) and catalase (CAT) level in colon and serum compared with DSS group. Sodium propionate inhibited macrophages with CD68 marker infiltration into the colonic mucosa of colitis mice. These results suggest that oral administration of sodium propionate could ameliorate DSS-induced colitis mainly by improving intestinal barrier function and reducing inflammation and oxidative stress via the STAT3 signaling pathway.
first_indexed 2024-04-12T17:49:26Z
format Article
id doaj.art-ea71d0dd8d6047338a7835b6a5c9dc0e
institution Directory Open Access Journal
issn 1663-9812
language English
last_indexed 2024-04-12T17:49:26Z
publishDate 2016-08-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Pharmacology
spelling doaj.art-ea71d0dd8d6047338a7835b6a5c9dc0e2022-12-22T03:22:32ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122016-08-01710.3389/fphar.2016.00253202262Propionate ameliorates dextran sodium sulfate-induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stressLingchang Tong0Lingchang Tong1Yue Wang2Yue Wang3Zhi-bin Wang4Wei-ye Liu5Sheng Sun6Li-chao Zhang7Ding-feng Su8LING LI9Shanghai Municipal Hospital of Traditional Chinese MedicineSecond Military Medical UniversityNingxia Medical UniversityShanghai Municipal Hospital of Traditional Chinese MedicineSecond Military Medical UniversitySecond Military Medical UniversitySecond Military Medical UniversityShanghai Municipal Hospital of Traditional Chinese MedicineSecond Military Medical UniversitySecond Military Medical UniversityPropionate is a short chain fatty acid and abundant as butyrate in the gut and blood. However, propionate has been studied less extensively than butyrate in the treatment of colitis. The present study was to investigate the effects of sodium propionate on intestinal barrier function, inflammation and oxidative stress in dextran sulfate sodium (DSS)-induced mice. Animals in DSS group received drinking water from 1 to 6 days and DSS (3% (w/v) dissolved in double distilled water) instead of drinking water from 7 to 14 days. Animals in DSS+Prop group were given 1% sodium propionate for 14 consecutive days and supplemented with 3% DSS solution on day 7-14. Intestinal barrier function, proinflammatory factors, oxidative stress, and signal transducer and activator of transcription 3 (STAT3) signaling pathway in the colon were determined. It was found that sodium propionate ameliorated body weight loss, colon-length shortening and colonic damage in colitis mice. Sodium propionate significantly inhibited the increase of FITC-dextran in serum and the decrease of zonula occludens-1 (ZO-1), occludin and E-cadherin expression in the colonic tissue. It also inhibited the expression of interleukin (IL)-1β, IL-6 and tumor necrosis factor-α (TNF-α) mRNA and phosphorylation of STAT3 in colitis mice markedly, reduced the myeloperoxidase (MPO) level, and increased the superoxide dismutase (SOD) and catalase (CAT) level in colon and serum compared with DSS group. Sodium propionate inhibited macrophages with CD68 marker infiltration into the colonic mucosa of colitis mice. These results suggest that oral administration of sodium propionate could ameliorate DSS-induced colitis mainly by improving intestinal barrier function and reducing inflammation and oxidative stress via the STAT3 signaling pathway.http://journal.frontiersin.org/Journal/10.3389/fphar.2016.00253/fullInflammationulcerative colitisintestinal barrier functionshort-chain fatty acidpropionateDextran sulfate sodium
spellingShingle Lingchang Tong
Lingchang Tong
Yue Wang
Yue Wang
Zhi-bin Wang
Wei-ye Liu
Sheng Sun
Li-chao Zhang
Ding-feng Su
LING LI
Propionate ameliorates dextran sodium sulfate-induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stress
Frontiers in Pharmacology
Inflammation
ulcerative colitis
intestinal barrier function
short-chain fatty acid
propionate
Dextran sulfate sodium
title Propionate ameliorates dextran sodium sulfate-induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stress
title_full Propionate ameliorates dextran sodium sulfate-induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stress
title_fullStr Propionate ameliorates dextran sodium sulfate-induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stress
title_full_unstemmed Propionate ameliorates dextran sodium sulfate-induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stress
title_short Propionate ameliorates dextran sodium sulfate-induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stress
title_sort propionate ameliorates dextran sodium sulfate induced colitis by improving intestinal barrier function and reducing inflammation and oxidative stress
topic Inflammation
ulcerative colitis
intestinal barrier function
short-chain fatty acid
propionate
Dextran sulfate sodium
url http://journal.frontiersin.org/Journal/10.3389/fphar.2016.00253/full
work_keys_str_mv AT lingchangtong propionateamelioratesdextransodiumsulfateinducedcolitisbyimprovingintestinalbarrierfunctionandreducinginflammationandoxidativestress
AT lingchangtong propionateamelioratesdextransodiumsulfateinducedcolitisbyimprovingintestinalbarrierfunctionandreducinginflammationandoxidativestress
AT yuewang propionateamelioratesdextransodiumsulfateinducedcolitisbyimprovingintestinalbarrierfunctionandreducinginflammationandoxidativestress
AT yuewang propionateamelioratesdextransodiumsulfateinducedcolitisbyimprovingintestinalbarrierfunctionandreducinginflammationandoxidativestress
AT zhibinwang propionateamelioratesdextransodiumsulfateinducedcolitisbyimprovingintestinalbarrierfunctionandreducinginflammationandoxidativestress
AT weiyeliu propionateamelioratesdextransodiumsulfateinducedcolitisbyimprovingintestinalbarrierfunctionandreducinginflammationandoxidativestress
AT shengsun propionateamelioratesdextransodiumsulfateinducedcolitisbyimprovingintestinalbarrierfunctionandreducinginflammationandoxidativestress
AT lichaozhang propionateamelioratesdextransodiumsulfateinducedcolitisbyimprovingintestinalbarrierfunctionandreducinginflammationandoxidativestress
AT dingfengsu propionateamelioratesdextransodiumsulfateinducedcolitisbyimprovingintestinalbarrierfunctionandreducinginflammationandoxidativestress
AT lingli propionateamelioratesdextransodiumsulfateinducedcolitisbyimprovingintestinalbarrierfunctionandreducinginflammationandoxidativestress