Colon Expression of Chemokines and Their Receptors Depending on the Stage of and Oat Beta-Glucan Dietary Intervention-Crohn's Disease Model Study

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2022 Feb 15

PMID 35163326

Authors

Lukasz Kopiasz

Katarzyna Dziendzikowska

Joanna Gromadzka-Ostrowska

Affiliations

Soon will be listed here.

Abstract

Crohn's disease (CD), a condition characterized by chronic inflammation of the gastrointestinal tract with alternating periods of exacerbation and remission, is becoming common around the world. This study aimed to analyze the molecular mechanisms underlying the anti-inflammatory properties of oat beta-glucans of varying molar masses by modulating the expression of chemokines and their receptors as well as other proteins related to both stages of TNBS (2,4,6-trinitrobenzosulfonic acid)-induced , which is an animal model of CD. The experiment involved 96 Sprague-Dawley rats, which were divided into two main groups: control and TNBS-induced . Both groups of rats were further divided into three dietary subgroups, which were fed with standard feed or feed supplemented with low- or high-molar-mass oat beta-glucans for 3 (reflecting acute inflammation) or 7 days (reflecting pre-remission). The gene expression of chemokines and their receptors in the colon wall was determined by RT-PCR, and the expression of selected proteins in the mucosa was determined by immunohistochemical analysis. The results showed that acute and pre-remission stages of were characterized by the increased gene expression of seven chemokines and four chemokine receptors in the colon wall as well as disrupted protein expression of CXCL1, CCL5, CXCR2, CCR5, and OPN in the mucosa. The consumption of oat beta-glucans resulted in decreased expression of most of these genes and modulated the expression of all proteins, with a stronger effect observed with the use of high-molar-mass beta-glucan. To summarize, dietary oat beta-glucans, particularly those of high molar mass, can reduce by modulating the expression of chemokines and their receptors and certain proteins associated with CD.

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References

Cheluvappa R, Thomas D, Selvendran S . The Role of Specific Chemokines in the Amelioration of Colitis by Appendicitis and Appendectomy. Biomolecules. 2018; 8(3). PMC: 6165111. DOI: 10.3390/biom8030059. View

Tang R, Yang G, Zhang S, Wu C, Chen M . Opposite effects of interferon regulatory factor 1 and osteopontin on the apoptosis of epithelial cells induced by TNF-α in inflammatory bowel disease. Inflamm Bowel Dis. 2014; 20(11):1950-61. DOI: 10.1097/MIB.0000000000000192. View

Savic Mlakar A, Hojsak I, Jergovic M, Cimic S, Bendelja K . Pediatric Crohn disease is characterized by Th1 in the terminal ileum and Th1/Th17 immune response in the colon. Eur J Pediatr. 2018; 177(4):611-616. DOI: 10.1007/s00431-017-3076-8. View

Kostova Z, Batsalova T, Moten D, Teneva I, Dzhambazov B . Ragweed-allergic subjects have decreased serum levels of chemokines CCL2, CCL3, CCL4 and CCL5 out of the pollen season. Cent Eur J Immunol. 2016; 40(4):442-6. PMC: 4737740. DOI: 10.5114/ceji.2015.56965. View

Hamilton J, Cook A, Tak P . Anti-colony-stimulating factor therapies for inflammatory and autoimmune diseases. Nat Rev Drug Discov. 2016; 16(1):53-70. DOI: 10.1038/nrd.2016.231. View

Hong S, Joung J, Bae J, Lee C, Koo J, Park S . RNA-seq Reveals Transcriptomic Differences in Inflamed and Noninflamed Intestinal Mucosa of Crohn's Disease Patients Compared with Normal Mucosa of Healthy Controls. Inflamm Bowel Dis. 2017; 23(7):1098-1108. DOI: 10.1097/MIB.0000000000001066. View

Antoniou E, Margonis G, Angelou A, Pikouli A, Argiri P, Karavokyros I . The TNBS-induced colitis animal model: An overview. Ann Med Surg (Lond). 2016; 11:9-15. PMC: 5021709. DOI: 10.1016/j.amsu.2016.07.019. View

Li M, Sun X, Zhao J, Xia L, Li J, Xu M . CCL5 deficiency promotes liver repair by improving inflammation resolution and liver regeneration through M2 macrophage polarization. Cell Mol Immunol. 2019; 17(7):753-764. PMC: 7331700. DOI: 10.1038/s41423-019-0279-0. View

Piovezani Ramos G, Papadakis K . Mechanisms of Disease: Inflammatory Bowel Diseases. Mayo Clin Proc. 2019; 94(1):155-165. PMC: 6386158. DOI: 10.1016/j.mayocp.2018.09.013. View

10.

Yu C, Zhang S, Wang Y, Zhang S, Luo L, Thorlacius H . Platelet-Derived CCL5 Regulates CXC Chemokine Formation and Neutrophil Recruitment in Acute Experimental Colitis. J Cell Physiol. 2015; 231(2):370-6. DOI: 10.1002/jcp.25081. View

11.

Iida T, Wagatsuma K, Hirayama D, Nakase H . Is Osteopontin a Friend or Foe of Cell Apoptosis in Inflammatory Gastrointestinal and Liver Diseases?. Int J Mol Sci. 2017; 19(1). PMC: 5795959. DOI: 10.3390/ijms19010007. View

12.

Li Q, Lian Y, Deng Y, Chen J, Wu T, Lai X . mRNA-engineered mesenchymal stromal cells expressing CXCR2 enhances cell migration and improves recovery in IBD. Mol Ther Nucleic Acids. 2021; 26:222-236. PMC: 8413681. DOI: 10.1016/j.omtn.2021.07.009. View

13.

Kopiasz L, Dziendzikowska K, Gajewska M, Wilczak J, Harasym J, Zyla E . Time-Dependent Indirect Antioxidative Effects of Oat Beta-Glucans on Peripheral Blood Parameters in the Animal Model of Colon Inflammation. Antioxidants (Basel). 2020; 9(5). PMC: 7278816. DOI: 10.3390/antiox9050375. View

14.

Oz H, Zhong J, de Villiers W . Osteopontin ablation attenuates progression of colitis in TNBS model. Dig Dis Sci. 2011; 57(6):1554-61. DOI: 10.1007/s10620-011-2009-z. View

15.

Xiao H, Peng J, Wen B, Hu D, Hu X, Shen X . Indigo Naturalis Suppresses Colonic Oxidative Stress and Th1/Th17 Responses of DSS-Induced Colitis in Mice. Oxid Med Cell Longev. 2019; 2019:9480945. PMC: 6815543. DOI: 10.1155/2019/9480945. View

16.

Chen L, Deng H, Cui H, Fang J, Zuo Z, Deng J . Inflammatory responses and inflammation-associated diseases in organs. Oncotarget. 2018; 9(6):7204-7218. PMC: 5805548. DOI: 10.18632/oncotarget.23208. View

17.

Zyla E, Dziendzikowska K, Gajewska M, Wilczak J, Harasym J, Gromadzka-Ostrowska J . Beneficial Effects of Oat Beta-Glucan Dietary Supplementation in Colitis Depend on its Molecular Weight. Molecules. 2019; 24(19). PMC: 6804032. DOI: 10.3390/molecules24193591. View

18.

Le Berre C, Ananthakrishnan A, Danese S, Singh S, Peyrin-Biroulet L . Ulcerative Colitis and Crohn's Disease Have Similar Burden and Goals for Treatment. Clin Gastroenterol Hepatol. 2019; 18(1):14-23. DOI: 10.1016/j.cgh.2019.07.005. View

19.

Girbl T, Lenn T, Perez L, Rolas L, Barkaway A, Thiriot A . Distinct Compartmentalization of the Chemokines CXCL1 and CXCL2 and the Atypical Receptor ACKR1 Determine Discrete Stages of Neutrophil Diapedesis. Immunity. 2018; 49(6):1062-1076.e6. PMC: 6303217. DOI: 10.1016/j.immuni.2018.09.018. View

20.

Aldinucci D, Colombatti A . The inflammatory chemokine CCL5 and cancer progression. Mediators Inflamm. 2014; 2014:292376. PMC: 3910068. DOI: 10.1155/2014/292376. View