Red Cabbage Juice-Mediated Gut Microbiota Modulation Improves Intestinal Epithelial Homeostasis and Ameliorates Colitis

Author:

Jean Wilson Emily1,Sirpu Natesh Nagabhishek23ORCID,Ghadermazi Parsa4ORCID,Pothuraju Ramesh5,Prajapati Dipakkumar R.6ORCID,Pandey Sanjit7,Kaifi Jussuf T.8ORCID,Dodam John R.2,Bryan Jeffrey N.2,Lorson Christian L.9ORCID,Watrelot Aude A.10ORCID,Foster Jason M.11,Mansell Thomas J.12ORCID,Joshua Chan Siu Hung4ORCID,Batra Surinder K.5ORCID,Subbiah Jeyamkondan13,Rachagani Satyanarayana23

Affiliation:

1. Department of Biological Systems Engineering, University of Nebraska-Lincoln, Lincoln, NE 68583, USA

2. Department of Veterinary Medicine and Surgery, University of Missouri, Columbia, MO 65201, USA

3. Roy Blunt NextGen Precision Health Institute, University of Missouri, Columbia, MO 65211, USA

4. Department of Chemical and Biological Engineering, Colorado State University, Fort Collins, CO 80523, USA

5. Department of Biochemistry and Molecular Biology, University of Nebraska Medical Center, Omaha, NE 68198, USA

6. Department of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, NE 68198, USA

7. Department of Genetics, Cell Biology and Anatomy, University of Nebraska Medical Center, Omaha, NE 68198, USA

8. Department of Surgery, School of Medicine, University of Missouri, Columbia, MO 65211, USA

9. Department of Veterinary Pathobiology, University of Missouri, Columbia, MO 65211, USA

10. Department of Food Science and Human Nutrition, Iowa State University, Ames, IA 50011, USA

11. Department of Surgery, Division of Surgical Oncology, University of Nebraska Medical Center, Omaha, NE 68198, USA

12. Department of Chemical and Biological Engineering, Iowa State University, Ames, IA 50011, USA

13. Department of Food Science, University of Arkansas, Fayetteville, AR 72701, USA

Abstract

Gut microbiota plays a crucial role in inflammatory bowel diseases (IBD) and can potentially prevent IBD through microbial-derived metabolites, making it a promising therapeutic avenue. Recent evidence suggests that despite an unclear underlying mechanism, red cabbage juice (RCJ) alleviates Dextran Sodium Sulfate (DSS)-induced colitis in mice. Thus, the study aims to unravel the molecular mechanism by which RCJ modulates the gut microbiota to alleviate DSS-induced colitis in mice. Using C57BL/6J mice, we evaluated RCJ’s protective role in DSS-induced colitis through two cycles of 3% DSS. Mice were daily gavaged with PBS or RCJ until the endpoint, and gut microbiota composition was analyzed via shotgun metagenomics. RCJ treatment significantly improved body weight (p ≤ 0.001), survival in mice (p < 0.001) and reduced disease activity index (DAI) scores. Further, RCJ improved colonic barrier integrity by enhancing the expression of protective colonic mucins (p < 0.001) and tight junction proteins (p ≤ 0.01) in RCJ + DSS-treated mice compared to the DSS group. Shotgun metagenomic analysis revealed an enrichment of short-chain fatty acids (SCFAs)-producing bacteria (p < 0.05), leading to increased Peroxisome Proliferator-Activated Receptor Gamma (PPAR-γ) activation (p ≤ 0.001). This, in turn, resulted in repression of the nuclear factor κB (NFκB) signaling pathway, causing decreased production of inflammatory cytokines and chemokines. Our study demonstrates colitis remission in a DSS-induced mouse model, showcasing RCJ as a potential modulator for gut microbiota and metabolites, with promising implications for IBD prevention and treatment.

Funder

National Science Foundation

Nebraska Research Initiative

National Institute of Health

Colorado State University

Publisher

MDPI AG

Subject

Inorganic Chemistry,Organic Chemistry,Physical and Theoretical Chemistry,Computer Science Applications,Spectroscopy,Molecular Biology,General Medicine,Catalysis

Reference96 articles.

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3. (2023, April 05). IBD Statistics 2022: Crohn’s and Ulcerative Colitis. Available online: https://ampersandhealth.co.uk/myibdcare/resources/ibd-statistics-2022-crohns-and-ulcerative-colitis/.

4. SCFAs—The thin microbial metabolic line between good and bad;Serino;Nat. Rev. Endocrinol.,2019

5. Inflammatory Bowel Disease in Children and Adolescents;Rosen;JAMA Pediatr.,2015

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